The case for chiropteran monophyly

AMERICAN MUSEUM
Novitates

PUBLISHED BY THE AMERICAN MUSEUM OF NATURAL HISTORY
CENTRAL PARK WEST AT 79TH STREET, NEW YORK, N.Y. 10024

Number 3103, 54 pp., 8 figures, 5 tables June 24, 1994

The Case for Chiropteran Monophyly

NANCY B. SIMMONS!

CONTENTS
PUDSIT ACT ie Un Ma Rie Be iene Bek cle Beet ihn g isp oes ara eden co slgt Mm ad, 4 eeRB a geieod ane ages saw ted 2
PWT OE UCT Oia Rica ae eae oer ed oaens, oo LE he) ee Pe Fee 2
Microchiroptera and Megachiroptera ............0.00 0.002. n eas 2
Origins of the Bat Monophyly Controversy .................... Seah be ede taren eee ein 3
Review of Phylogenetic Studies? 05.5255 84.4) toe ones oo Bed Seow nels esha 4
FaxOmomic Sampling: <i. cee ihe vce tele purge ack, soy ep abe actin oF Sek AER ERIe op ed eat weep alle rence eee 5
Results of Biochemical and Molecular Studies ............ 0.0.0.0. c cece eee ene 6
Results of Morphological Studies ..........0.0..0. 000 ccc cc ene e eens 13
Results of Studies Combining Morphological and Molecular Data ................. 18
STAT Yih nte sh ash wood eA re rangi ee asthe, tiem EPA ihe oh ee oS Fa. O Sa OG oat, 18
Morphological Characters Supporting Bat Monophyly .........................0005 19
NSTC ERCIT 5 Fs N cco eh ea ed tees ae ns oR Pe OL ee: Bo ee ee 19
Skull and Cranial Vascular System .......... 0.0.0.0... 000 ccc cece eee eee eens 20
Postcranial Musculoskeletal System .............0. 0.0000. ccc cece cece eee nee 24
Fetal Membranes’ tances i455 as cetiocicne le, eS, Geanlone dee seme EE Lh ean 6B, ose 34
ING VOUS Sy SCSI 2 Fhe ee on coronas Aigtaad areca tale scinseabicwurne ore abate pital seh bebtieg Bete aetis 37
Rejected Putative Synapomorphies ............ 00.0.0. ccc eee eee ee eee eee nenees 38
Discussion and Conclusions .............00 0.000 c cece ee cence nee e nese ences 42
What is the Sister Group of Bats? .......000 0.00. cee nee enneenas 42
Directions for Future Research ...........0.0.. 0.0. c cc cece ee eee eee eee cece enaeas 44
Acknowledemenits: - 44" Jeet p Eh eo} tee bad eho ed ea deed et ee og 46
References: 9 vt256.5.0 Boer rcvcs SRPMS ee OPT. Nearemetig INES sy Auge bent ABW ook cue tee Olyeta hie 46

’ Assistant Curator, Department of Mammalogy, American Museum of Natural History.

Copyright © American Museum of Natural History 1994 ISSN 0003-0082 / Price $6.00

2 AMERICAN MUSEUM NOVITATES

NO. 3103

ABSTRACT

The current controversy concerning bat mono-
phyly centers on relationships of Microchiroptera,
Megachiroptera, Primates, and several other groups
of mammals. Despite claims to the contrary, stud-
ies of both molecular and morphological data
strongly support bat monophyly and a single origin
for powered flight in mammals. Analyses of some
molecular data sets have yielded inconclusive re-
sults (e.g., rDNA restriction sites, aA-crystallin
amino acid sequences, and cytochrome oxidase
subunit I gene nucleotide sequences). However,
analyses of most biochemical and molecular data
support monophyly of bats (e.g., albumin im-
munological distances, DNA-DNA hybridization,
a-globin + 8-globin amino acid sequences, nucle-
otide sequence data from the e-globin gene, inter-
photoreceptor retinoid binding protein gene, 12S

rRNA gene, and cytochrome oxidase subunit II
gene). In no instance have molecular data provid-
ed unambiguous support for bat diphyly. Mor-
phological data show a slightly different pattern.
Neural and penial characters support diphyly of
bats, but other data subsets clearly support bat
monophyly (e.g., characters of the cranium and
postcranial skeleton, vascular system, muscles, and
fetal membranes). When all of the morphological
data are considered together, the combined data
set strongly supports bat monophyly. Over 25
morphological synapomorphies— many of which
consist of complex suites of modifications—di-
agnose the monophyletic order Chiroptera. The
fact that these synapomorphies represent many
different anatomical systems further strengthens
the case for chiropteran monophyly.

INTRODUCTION

Monophyly of Chiroptera—and a single or-
igin for powered flight in mammals—has been
assumed by most evolutionary biologists be-
cause all bats apparently share a unique set
of specializations for flight. However, bat
monophyly and homology of the chiropteran
wing have been questioned by authors who
have suggested that Megachiroptera and Mi-
crochiroptera may not be sister taxa (Jones
and Genoways, 1970; Smith, 1976, 1980;
Smith and Madkour, 1980; Hill and Smith,
1984; Pettigrew, 1986, 1991a, 1991b; Petti-
grew and Jamieson, 1987; Pettigrew et al.,
1989). If the two major bat lineages are only
distantly related and their most recent com-
mon ancestor was nonvolant, then a dual or-
igin for wings and powered flight within
Mammalia must be hypothesized.

Bat diphyly and related hypotheses (e.g.,
megachiropterans as “‘flying primates’’) have
been the focus of intense discussion in recent
years, with some authors defending the tra-
ditional concept of a monophyletic Chirop-
tera (e.g., Wible and Novacek, 1988) while
others supported bat diphyly (e.g., Pettigrew
et al., 1989). In 1991 the controversy was
reviewed in a series of papers that appeared
together in Systematic Zoology (i.e., Baker et
al., 1991b; Pettigrew, 1991la, 1991b; Sim-
mons et al., 1991). At that time, much of the
relevant data remained unpublished, includ-

ing several significant molecular studies. As
a result, the controversy remained largely un-
resolved. However, since that time over a
dozen new phylogenetic studies have been
published (tables 1, 2, 3), and the data sup-
porting different phylogenetic hypotheses
have been further critiqued (e.g., Thiele et
al., 1991; Johnson and Kirsch, 1993; Kaas
and Preuss, 1993; Simmons, 1993). These
studies have added considerably to our
knowledge and understanding of relevant data
and methodological issues, and have set the
stage for resolution of the debate.

MICROCHIROPTERA AND MEGACHIROPTERA

In any phylogenetic argument it is impor-
tant that the taxa under consideration (the
“operational taxonomic units”) be mono-
phyletic. One aspect of bat systematics that
has not been the source of controversy is the
status of the two bat suborders—there is gen-
eral agreement that Megachiroptera and Mi-
crochiroptera are each monophyletic taxa
(Smith, 1976, 1980; Van Valen, 1979; No-
vacek, 1980b, 1987; Pettigrew et al., 1989;
Pettigrew, 1991a, 1991b; Baker et al., 199 1a,
1991b; Kay et al., 1992; Beard, 1993a).
Monophyly of Microchiroptera has rarely
been questioned because all members of the
group share a unique system of laryngeal

1994 SIMMONS: CHIROPTERAN MONOPHYLY 3

echolocation (Fleischer, 1973, 1978; Hill and
Smith, 1984; Novacek, 1987; Pettigrew et al.,
1989). Many cetaceans also use sophisticated
echolocation, but the anatomical basis of the
system is quite different (Fleischer, 1973,
1978). In addition to features related to echo-
location, all microchiropterans share a unique
arrangement of the gray matter in the spinal
cord plus several apomorphic features of the
cranium and postcranium (Van Valen, 1979;
Novacek, 1987; Pettigrew et al., 1989; Kay
et al., 1992; Beard, 1993a).

Megachiroptera also appears to be mono-
phyletic. Extant megachiropterans share den-
tal specializations associated with frugivory
(Slaughter, 1970; Koopman and MacIntyre,
1980), an unusual bilobed keel on the ma-
nubrium (personal obs.), and sperm with sev-
eral unique structural features (Rouse and
Robson, 1986). In addition, the nutrient sys-
tem of the megachiropteran retina involves
a pattern of invasive choroid papillae that is
not found in any other vertebrate (Kolmer,
1910, 1911, 1926; Fritsch, 1911; Duke-En-
dler, 1958; Pedler and Tilley, 1969; Buttery
et al., 1990).

A number of well-preserved Eocene fossils
provide our earliest record of bat evolution.
Several taxa (e.g., Icaronycteris, Palaeochi-
ropteryx) once considered to be possible an-
cestors of all extant bats are now believed to
represent early branches of the microchirop-
teran lineage (Novacek, 1985a, 1987; Ha-
bersetzer and Storch, 1987, 1992). Charac-
ters supporting placement of these taxa in
Microchiroptera include features of the ear,
basicranium, dentition, and postcranial skel-
eton (Novacek, 1985a, 1987). Although many
fossils are too fragmentary to assess for most
of these characters, dental morphology sug-
gests that virtually all Eocene bats currently
known belong to Microchiroptera. One ex-
ception is a specimen from the Late Eocene
of Thailand, an isolated tooth which appears
to be a lower premolar of a megachiropteran
bat (Ducrocg et al., 1993).

The best-preserved putative megachirop-
teran is Archaeopteropus, which is known only
from a single partial skeleton from the Late
Oligocene of Italy (Meschinelli, 1903). The
skull and dentition of this specimen are badly
damaged, but some evidence suggests that
Archaeopteropus might have had an insectiv-

orous-type dentition (Revilliod, 1922; Rus-
sell and Sigé, 1970; Slaughter, 1970). Nev-
ertheless, Archaeopteropus is widely regarded
to be a megachiropteran because of similar-
ities in wing morphology shared by this taxon
and extant megachiropterans (Anderson,
1912; Revilliod, 1922; Dal Piaz, 1937; Ha-
bersetzer and Storch, 1987).

Consideration of the fossil record indicates
that the lineages leading to extant megachi-
ropterans and microchiropterans have been
separated since at least the Late Eocene, over
50 million years. During this time a great deal
of molecular and morphological evolution has
taken place, complicating efforts to resolve
higher-level relationships (Baker et al., 199 1a,
1991b). Many significant morphological, be-
havioral, and genetic differences exist be-
tween Megachiroptera and Microchiroptera
(Jones and Genoways, 1970; Pettigrew et al.,
1989; Sabeur et al., 1993). Despite these dif-
ferences, monophyly of bats was more or less
assumed between the time Chiroptera was
named by Blumenbach (1779) and the early
1970s, when doubts were first raised con-
cerning the evolutionary origins of bats
(Gregory, 1910; Simpson, 1945; Jones and
Genoways, 1970; Smith, 1980).

ORIGINS OF THE BAT MONOPHYLY
CONTROVERSY

Jones and Genoways (1970) were the first
to explicitly suggest that Chiroptera might be
diphyletic. They discussed the differences be-
tween Megachiroptera and Microchiroptera,
and pointed out that similarities between
these taxa principally involve the flight
mechanism. This raised the prospect that
“convergent evolution attendant with devel-
opment of aerial locomotion” —rather than
shared ancestry—might account for similar-
ities between megachiropteran and micro-
chiropteran bats (Jones and Genoways, 1970:
5). This idea was further discussed by Smith
(1976, 1980), and the first data supporting
bat diphyly were presented by Smith and
Madkour (1980). Subsequent discussions
have focused on relationships of Megachi-
roptera and Microchiroptera to each other
and to other mammalian groups, particularly
various “‘archontan’? mammals including
Primates, Dermoptera (colugos or gliding le-

4 AMERICAN MUSEUM NOVITATES

murs), Scandentia (tree shrews), and extinct
Plesiadapidae and Paromomyidae (fossil
forms generally considered related to either
primates or dermopterans). With the possible
exception of Paromomyidae, all of these taxa
appear to be monophyletic (Zeller, 1986; Wi-
ble and Covert, 1987; Kay etal., 1992; Beard,
1993a).

Smith and Madkour (1980) identified six
derived morphological characters that Mega-
chiroptera shares with archontan taxa other
than Microchiroptera, including features of
the penis, brain, wrist, and dentition. Inad-
equate character descriptions and lack of ev-
idence for homology of some derived char-
acter states compromised the results of their
phylogenetic analysis (see discussion under
Results of Morphological Studies), and few
systematists accepted Smith and Madkour’s
(1980) conclusion that bats are diphyletic.
Hill and Smith (1984) favored the diphyly
hypothesis but presented no new data.

In the late 1980s Pettigrew and his col-
leagues reported a series of derived features
of the nervous system that support chirop-
teran diphyly. The phylogeny they presented
suggests that Megachiroptera is more closely
related to Primates and Dermoptera than it
is to Microchiroptera, which falls well outside
‘‘Archonta” and may represent one of the
most basal branches within Eutheria (Petti-
grew, 1986, 199la, 1991b; Pettigrew and
Cooper, 1986; Pettigrew and Jamieson, 1987;
Pettigrew et al., 1989), Over 20 derived neu-
ral traits and one postcranial character have
been cited as supporting this hypothesis, al-
though some of these features have yet to be
studied in all of the relevant taxa (see sum-
mary in Pettigrew, 1991a). Methods of phy-
logenetic analysis and details of several char-
acters employed by Pettigrew and his
colleagues have been questioned by various
authors (e.g., Wible and Novacek, 1988; Ba-
ker et al., 1991b; Simmons et al., 1991; Thiele
et al., 1991; Johnson and Kirsch, 1993; Kaas
and Preuss, 1993; Simmons, 1993). How-
ever, aspects of the neural data are compel-
ling, and subsequent debate of Pettigrew’s
conclusions stimulated many morphological
and molecular studies (tables 1, 2, 3).

In part as a result of historical development
of the controversy, some authors in recent
years have treated “‘bat diphyly” as synon-

NO. 3103

ymous with Pettigrew’s hypothesis of rela-
tionships (i.e., Megachiroptera is more close-
ly related to Primates and Dermoptera than
to Microchiroptera). This overlooks the pos-
sibility that Megachiroptera might be related
to an entirely different set of taxa; Pettigrew
and his colleagues might be correct about bat
diphyly, yet wrong about the relationships of
Megachiroptera and Microchiroptera to oth-
er mammals. To avoid confusion between
the general concept of bat diphyly and Pet-
tigrew’s hypothesis of relationships, the
phrase “bat diphyly sensu Pettigrew et al.
(1989)” is used in the following discussions
to specify the phylogenetic hypothesis sup-
ported by Pettigrew and his colleagues.

REVIEW OF PHYLOGENETIC
STUDIES

Many different types of molecular and
morphological data have been used in studies
relevant to the bat monophyly controversy
(tables 1, 2). Some studies have focused on
data from a single protein, gene, or organ
system, while others have attempted to in-
tegrate diverse types of data. In general, two
categories of data may be recognized: dis-
tance data and discrete character data.

Distance data consist of measurements of
continuous variables estimated in a series of
pairwise comparisons. The “evolutionary
distance”’ separating taxa is calculated at the
end of a study by combining data from the
comparisons to form a consensus hypothesis.
Distance techniques (e.g., immunodiffusion,
DNA-DNA hybridization) offer methods for
estimating relationships among taxa, but un-
fortunately provide few means of evaluating
the nature of the evidence supporting various
relationships. Goodness-of-fit statistics may
be employed to evaluate trees, and replica-
tions may be performed to calculate confi-
dence limits, but problems exist with under-
lying assumptions of additivity of distances
(Felsenstein, 1984). Distance data do not per-
mit formulation or testing of hypotheses of
homology, and patterns of transformation
cannot be investigated. Subsets of data from
different sources cannot be combined, and it
is dificult to compare results of distance anal-
yses with those of discrete character analyses
except to note general agreement or disagree-

1994

ment concerning phylogenetic results (i.e., tree
topology). Nevertheless, distance techniques
provide a valid means for constructing phy-
logenies (Felsenstein, 1984; Sarich, 1993), and
some studies involving distance data are rel-
evant to the issue of bat monophyly.

In contrast to distance techniques, analyses
of discrete character data (e.g., morphological
traits, amino acid sequences, nucleotide se-
quences) require formulation and testing of
explicit hypotheses of homology. Subsets of
data from different sources (e.g., anatomical
systems) can be combined in comprehensive
analyses or analyzed separately depending on
the goals of the study. When phylogenetic
analyses have been completed, both tree to-
pology and the evidence supporting various
clades (i.e., synapomorphies) can be exam-
ined, and results of different studies can be
compared. Levels of homoplasy in characters
supporting a given clade can be considered
when evaluating the strength of the overall
evidence supporting a particular phylogenet-
ic conclusion. However, analyses of discrete
character data are subject to their own set of
problems, including character dependence
and problems associated with various
weighting schemes. All such issues must be
considered when evaluating the results of
phylogenetic studies (see discussion in Sim-
mons, 1993).

TAXONOMIC SAMPLING

One methodological issue of prime impor-
tance in the bat monophyly controversy is
taxonomic sampling (Baker et al., 1991b;
Simmons, 1993). Both chiropteran suborders
present problems because of their enormous
diversity. Megachiroptera comprises over 150
extant species referred to a single family, and
Microchiroptera includes over 750 extant
species referred to 16 families (Koopman,
1993). Because these taxa are speciose, stud-
ies of higher-level relationships must settle
for sampling only a subset of the species in-
cluded in each group. This is also true for
other relevant taxa including Primates (233
species) and Scandentia (19 species; Groves,
1993; Wilson, 1993).

Not surprisingly, taxonomic sampling has
been highly uneven in studies relevant to bat
monophyly (tables 1, 2). Some studies have

SIMMONS: CHIROPTERAN MONOPHYLY 5

included only one species from each of the
bat suborders (e.g., Mindell et al., 1991), while
others have examined multiple species rep-
resenting most or all extant families (e.g.,
Smith and Madkour, 1980). Sampling of bats
in the majority of phylogenetic studies falls
somewhere between these extremes (tables 1,
2). Taxonomic sampling of other mamma-
lian orders has similarly varied. Represen-
tatives of each of the non-bat archontan or-
ders (Primates, Dermoptera, and Scandentia)
are represented in most recent studies be-
cause these taxa are central to the bat mono-
phyly controversy. However, sampling with-
in these groups has been uneven, and other
orders of mammals considered crucial by
some authors (e.g., Insectivora, Carnivora)
have been omitted entirely from many phy-
logenetic analyses (tables 1, 2). Studies rele-
vant to bat monophyly range from those in-
cluding representatives of only three
mammalian orders (e.g., Mindell et al., 1991)
to those including representatives of all of the
extant orders (e.g., Sarich, 1993).
Taxonomic sampling is often effectively
constrained by the type of data under con-
sideration. Among molecular studies, the time
and expense involved in nucleotide sequenc-
ing have apparently discouraged workers from
attempting to sample broadly (table 1), al-
though this is now changing with the in-
creased use of PCR and universal primers.
Studies involving amino acid sequence data
tend to include a much broader sample of
taxa because comparable data for many taxa
have been collected over the years in con-
junction with different projects (table 1; Cze-
lusniak et al., 1990). Among morphological
studies, types of characters that can be ob-
served only with intensive laboratory work
(e.g., neural characters, fetal membranes) are
generally surveyed in fewer taxa than data
which can be easily obtained from standard
museum preparations (e.g., craniodental
characters). Fossil taxa potentially relevant
to the question of bat monophyly (e.g., Zcar-
onycteris, paromomyids) can be considered
only in the context of morphological data sets
that include characters preserved in fossils
(e.g., craniodental characters, vascular fea-
tures associated with osteological features).
Breadth and intensity of taxonomic sam-
pling can affect the results of phylogenetic

6 AMERICAN MUSEUM NOVITATES

studies in several ways, influencing both to-
pology of trees and perceived support for var-
ious relationships (Gauthier et al., 1988;
Donoghue et al., 1989; Novacek, 1992b,
1994; Simmons, 1993). In studies relevant to
bat monophyly, taxonomic sampling does not
appear to have had much impact on one cen-
tral phylogenetic conclusion — virtually all of
these studies support monophyly of bats (ta-
bles 1, 2). However, different studies have
reached different conclusions concerning re-
lationships of Chiroptera to other mamma-
lian orders, results which appear to be due at
least in part to sampling effects (see Discus-
sion and Conclusions below). The perceived
support for bat monophyly (or any other clade
identified in a phylogenetic analysis) depends
upon the specific taxa considered and the rel-
ative “phylogenetic distance’”’ between the
groups included in the study. Poor sampling
within bats may falsely indicate that some
variable characters are fixed synapomorphies
of Chiroptera, or may suggest that characters
are ambiguous when they in fact are not. Poor
sampling of other mammalian orders may
have similar effects, and support for chirop-
teran monophyly may be over- or underes-
timated if the true sister group of bats (what-
ever taxon that may be) is absent from a study.
These possibilities indicate that sampling
methods must be considered when inter-
preting results of phylogenetic analyses.

RESULTS OF BIOCHEMICAL AND
MOLECULAR STUDIES

A wide variety of biochemical and molec-
ular data have been used in attempts to re-
solve bat relationships (table 1). Some studies
have produced inconclusive results, but the
majority support monophyly of Chiroptera.
In no case have molecular data provided un-
ambiguous support for bat diphyly.

IMMUNOLOGICAL DISTANCE DATA AND
DNA-DNA HyYBRIDIZATION

The use of immunological data in studies
of higher-level relationships of mammals was
reviewed recently by Sarich (1993). Cronin
and Sarich (1980) reported that albumin im-
munological distance data from bats and
members of four other mammalian orders
provide clear support for bat monophyly (ta-

NO. 3103

ble 1). Results of more comprehensive im-
munodiffusion experiments involving addi-
tional mammalian orders have never been
fully reported, but Sarich (1993: 105) stated
that results of such experiments “‘unequivo-
cally support bat monophyly.”

Kilpatrick and Nunez (1993) and Nunez
and Kilpatrick (in press) have reported in ab-
stracts the results of a DNA-DNA hybrid-
ization study that included bats and members
of three other mammalian orders (table 1).
Results of bootstrap analyses indicate some
ambiguity in the data (Kilpatrick and Nunez,
1993), but phylogenetic trees generated from
analysis of mean estimates of genetic diver-
gence and normalized percent of hybridiza-
tion were interpreted as supporting mono-
phyly of Chiroptera (Kilpatrick and Nunez,
1993; Nunez and Kilpatrick, in press).

AMINO ACID SEQUENCES

Pettigrew et al. (1989) were the first to use
amino acid sequence data to address rela-
tionships of Megachiroptera and Microchi-
roptera. A series of “preliminary”’ phyloge-
netic trees produced from analyses of 6-globin
amino acid sequences in bats and members
of seven other mammalian orders were in-
terpreted by Pettigrew et al. (1989) as sup-
porting bat diphyly. However, Baker et al.
(1991b) disagreed with that interpretation,
pointing out that diphyly of Microchiroptera
and Primates—rather than Chiroptera— was
indicated by topology of the 6-globin trees.
Pettigrew (199 1a) added several taxa (and ap-
parently some a-globin sequences) to the data
set, and upon reanalysis concluded that the
hemoglobin data are ambiguous concerning
bat relationships.

The hemoglobin studies discussed by Pet-
tigrew and his colleagues are difficult to in-
terpret because the data have never been pub-
lished, and it is not entirely clear which globin
sequences were considered by Pettigrew
(1991a). In other studies, Stanhope et al.
(1993) reported that analyses including both
a-globin and 8-globin amino acid sequences
provide support for bat monophyly. Stan-
hope et al. (1993) argued that Pettigrew
(1991a) had used exactly the same a-globin
and 6-globin data employed in their studies,
but that his analytical procedures had not

1994

allowed him to identify the most parsimo-
nious tree for the subset of taxa analyzed.
Stanhope et al.’s (1993) reanalysis of this data
subset (a- and 8-globin from 52 mammal spe-
cies) indicated monophyly of Chiroptera, al-
though support for this grouping was weak.
In trees only one step longer than the shortest
tree, two clades of bats (one containing ves-
pertilionids and another containing the re-
maining megachiropterans and microchirop-
terans) apparently occur as separate branches
at an unresolved node, thus suggesting that
both Chiroptera and Microchiroptera might
be paraphyletic. Bat monophyly sensu Pet-
tigrew et al. (1989) was not supported in any
of the near most parsimonious trees exam-
ined by Stanhope et al. (1993).

Analyses of more comprehensive amino
acid sequence data sets (including data from
a- and 6-globins, myoglobins, lens aA crys-
tallins, fibrinopeptides, cytochrome c, ribo-
nucleases, and embryonic a- and £-globins)
also provide weak support for bat monophyly
(Czelusniak et al., 1990; Stanhope et al.,
1993). A phylogenetic tree published by Cze-
lusniak et al. (1990: fig. 3) indicated para-
phyly of Chiroptera, but in the text (p. 565)
the authors noted that addition of a- and
G-globin data from another microchiropteran
(Tadarida) changes the tree topology so that
Chiroptera is monophyletic. The evidence
placing bats together within this tree must
have come principally from a- and 8-globin
data, as these were the only proteins sampled
in multiple bat species (Czelusniak et al.,
1990).

de Jong et al. (1993) reported results of a
study of aA-crystallin amino acid sequences
from bats and members of 17 other mam-
malian orders (table 1). Among the mammals
considered, sequence variation in the aA-
crystallin chain occurs at 62 positions (de Jong
et al., 1993: table 2.1), and substitutions at
32 of these positions may be phylogenetically
informative. Parsimony analysis of this data
set suggests bat diphyly, but only two addi-
tional steps are required to place bats together
in a monophyletic group (de Jong et al., 1993).
Because data from only three bat species
(Pteropus vampyrus, P. scapulatus, and Ar-
tibeus jamaicensis) were included in the study,
and only a single unambiguous sequence
transformation supported bat diphyly, de

SIMMONS: CHIROPTERAN MONOPHYLY 7

Jong et al. (1993: 9) concluded that the aA-
crystallin sequence data were “indecisive as
to the mono- or biphyletic origin of Micro-
and Megachiroptera.”’

rDNA RESTRICTION SITES

Baker et al. (1991a) mapped 52 rDNA re-
striction sites in bats and members of four
other mammalian orders (table 1). A total of
28 variable sites were identified, including 17
that were potentially phylogenetically infor-
mative (Baker et al., 1991a). Unfortunately,
relationships of Megachiroptera and Micro-
chiroptera could not be resolved using this
data set. A tree consistent with bat diphyly
sensu Pettigrew et al. (1989) was found to be
one step shorter than the bat monophyly tree
presented by Wible and Novacek (1988), but
this difference was interpreted as insignificant
(Baker et al., 1991a, 1991b). Parsimony anal-
ysis resulted in discovery of numerous trees
two steps shorter than the “‘bat diphyly”’ tree,
and a strict consensus of these produced a
poorly resolved tree which indicated non-
monophyly of Primates and Microchiroptera
as well as Chiroptera (Baker et al., 199 1a).
Pettigrew’s (1991a) claims to the contrary,
the rDNA restriction site data presented to
date do not appear to provide a useful guide
to higher-level relationships among archon-
tan mammals.

DNA SEQUENCES

Although most studies of DNA sequences
have included comparatively small numbers
of taxa (table 1), these studies have generally
produced conclusive results. Strong support
for bat monophyly has come from nucleotide
sequence analyses of two nuclear genes, the
e-globin gene (Bailey et al., 1992) and the gene
for interphotoreceptor retinoid binding pro-
tein (Stanhope et al., 1992, 1993). Chirop-
teran monophyly has also been supported by
analyses of nucleotide sequence data from
two mitochondrial genes, the cytochrome ox-
idase subunit II gene (Adkins and Honeycutt,
1991, 1993), and the 12S rDNA gene (Min-
dell et al., 1991; Ammerman and Hillis, 1992;
Knight and Mindell, 1993; Springer and
Kirsch, 1993).

Bailey et al. (1992) considered the nuclear
e-globin gene (the 5’-most member of the

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1994

G-globin gene cluster) to be appropriate for
investigating bat relationships because this
gene appears to have been less prone to tan-
dem duplications than other 6-type globin
genes, and because most of the e-globin se-
quence is noncoding and thus presumably not
subject to functional constraints. Over 1200
nucleotide positions of the «-globin sequence
were sampled in bats and members of five
other mammalian orders (table 1; Bailey et
al., 1992). Analysis of this data set resulted
in identification of a single most parsimo-
nious tree which supported monophyly of
Chiroptera (Bailey et al., 1992; Stanhope et
al., 1993). Trees indicating bat diphyly sensu
Pettigrew et al. (1989) were found to require
over 100 additional evolutionary steps (nu-
cleotide substitutions) than the shortest tree
(Bailey et al., 1992). Megachiroptera and Mi-
crochiroptera uniquely share 39 derived sub-
stitutions in the e-globin sequence, including
26 substitutions that exhibit no homoplasy
in the context of the data set (Bailey et al.,
1992; Stanhope et al., 1993). In contrast, only
two substitutions potentially support a mega-
chiropteran-primate clade or a megachirop-
teran-dermopteran clade.

The gene for interphotoreceptor retinoid
binding protein (IRBP) is a single-copy nu-
clear gene (Stanhope et al., 1992, 1993). Stan-
hope et al. (1992) argued that functionally
constrained coding DNA sequences such as
IRBP may be particularly useful for resolving
ancient phylogenetic branching patterns be-
cause the relatively low sequence divergence
seen in such genes facilitates alignment of
sequences from divergent mammalian or-
ders. IRBP sequences of approximately 1200
base pairs were collected from bats and mem-
bers of eight other mammalian orders (table
1; Stanhope et al., 1992). Analyses of these
data were conducted under a series of differ-
ent assumptions (neighbor-joining and par-
simony, rooted and unrooted trees, marsu-
pials present or absent in data set), and all
results strongly supported bat monophyly
(Stanhope et al., 1992). In an unrooted par-
simony analysis of the eutherian taxa, the
shortest tree indicating bat diphyly sensu Pet-
tigrew et al. (1989) required 46 more nucle-
otide substitutions than the most parsimo-
nious trees (Stanhope et al., 1992). A total of
22 nucleotide substitutions (7 of which were

SIMMONS: CHIROPTERAN MONOPHYLY 11

unique in the data set) were identified as syn-
apomorphies of Chiroptera (Stanhope et al.,
1992, 1993).

Adkins and Honeycutt (1991, 1993) com-
pared nucleotide sequences of 684 base pairs
of the mitochondrial cytochrome oxidase
subunit IIT gene (COII). The 1991 study in-
cluded two bat species and members of six
other mammalian orders; the 1993 version
included four bats and members of seven oth-
er orders (table 1). Analyses of the COII data
with transversions and transitions weighted
equally suggested chiropteran paraphyly in
both iterations of the study. In the 1991 anal-
ysis, a rodent nested within the smallest clade
containing both bats in the most parsimo-
nious trees (Adkins and Honeycutt, 1991: fig.
1A). In contrast, bats, primates, and artio-
dactyls formed a clade in four equally par-
simonious trees discovered in the 1993 study;
monophyly of Artiodactyla and Primates was
supported in all four of these trees, but Pri-
mates nested within the smallest clade con-
taining all four bats (Adkins and Honeycutt,
1993: fig. 3). Microchiroptera appeared as a
paraphyletic group in all equally parsimoni-
ous trees, with Rhinolophus appearing as the
sister taxon of Primates rather than grouping
with the other microchiropterans (Adkins and
Honeycutt, 1993). However, different results
were obtained when an alternative weighting
system was employed.

In both interations of Adkins and Honey-
cutt’s study, the most parsimonious trees
based on transversions-only data contained
a monophyletic Chiroptera. Ten nucleotide
substitutions supported Chiroptera in the
1991 study, while seven substitutions sup-
ported this group in the 1993 version (Adkins
and Honeycutt, 1991, 1993). In the 1993
study, which included three microchiropter-
ans, the topology reconstructed using the
transversions-only data is consistent with
current hypotheses of microchiropteran phy-
logeny (e.g., Van Valen, 1979; Luckett, 1980b;
Smith, 1980; Pierson, 1986). Microchirop-
tera forms a monophyletic group, and Mac-
rotus and Phyllostomus (members of the
monophyletic family Phyllostomidae) to-
gether form a well-supported clade within
Microchiroptera (Adkins and Honeycutt,
1993: fig. 3).

Studies of mitochondrial genes frequently

12 AMERICAN MUSEUM NOVITATES

employ transversion weighting, which is gen-
erally justified based on the expectation that
mitochondrial DNA transition/transversion
ratios decrease and transition substitutions
approach saturation as evolutionary diver-
gence increases (Adkins and Honeycutt, 1991;
Mindell et al., 1991). Because the divergence
times for bats and their possible relatives are
quite long (55-70 million years; Benton,
1990), transversion weighting has been judged
to be appropriate by most molecular system-
atists testing bat monophyly with mitochon-
drial DNA data (e.g., Adkins and Honeycutt,
1991, 1993; Mindell et al., 1991; Ammerman
and Hillis, 1992; Knight and Mindell, 1993;
Springer and Kirsch, 1993).

The technique most commonly used to ef-
fect transversion weighting is simple omis-
sion of transitions from the analysis (e.g., Ad-
kins and Honeycutt, 1991, 1993; Mindell et
al., 1991; Ammerman and Hillis, 1992).
However, questions have been raised re-
cently concerning this method (Springer and
Kirsch, 1993; Novacek, 1994; Wheeler, in
press). Sample size is one area of potential
weakness. Springer and Kirsch (1993) point-
ed out that transversion weighting may be
problematic when applied to short sequences
(e.g., <400 base pairs) because of the rela-
tively small number of transversions pre-
served in such sequences. Effectively dis-
carding potentially informative data (i.e.,
transitions) may be hard to justify in many
cases.

Wheeler (in press) and Novacek (1994) ad-
vocate application of a spectrum of weights
to transversions in order to discover the
threshold values that affect tree topologies.
Novacek (1994) reanalyzed the COII data
from Adkins and Honeycutt’s (1991) study
and found that bat monophyly was main-
tained when transversions were given weights
either 10 or 5 that of transitions, but the
bat clade collapsed when transversions were
weighted 2 transitions. The fact that rela-
tively low transversion/transition weighting
ratios (e.g., 5:1) produce trees in which Chi-
roptera is monophyletic may be interpreted
as providing strong support for bat mono-
phyly. ; .

Mindell et al. (1991) analyzed sequence data
from mitochondrial 12S rDNA (744 base
pairs) and cytochrome oxidase subunit I genes

NO. 3103

(COI; 236 base pairs) in two bats and mem-
bers of two other mammalian orders. Prelim-
inary analyses in which transitions and trans-
versions were weighted equally indicated that
bats were not monophyletic. However, when
only transversions were considered, Mindell
et al. (1991) found clear support for bat
monophyly even when the outgroup was var-
ied, alternative alignment strategies were em-
ployed, and a gap-coding scheme was used.
When the two data subsets were considered
separately, the 12S data strongly supported
bat monophyly, but the COI data were am-
biguous. Knight and Mindell (1993) exam-
ined the 12S data for substitution biases, and
found that transversions involving G (gua-
nine) were relatively rare and occurred far
below expected levels. Suggesting that these
rare substitutions may be particularly useful
for resolving branching patterns of ancient
divergences, Knight and Mindell (1993) not-
ed that two such transversions support bat
monophyly, while no substitutions of this type
support a megachiropteran + primate clade.

Ammerman and Hillis (1992) also ana-
lyzed mitochondrial 12S rDNA nucleotide
sequences. While Mindell et al. (1991) con-
sidered a relatively large number of base pairs,
the taxonomic sampling in that study was
very poor (table 1). In contrast, Ammerman
and Hillis (1992) considered a larger sample
of taxa (four bats and members of seven other
mammalian orders), but analyzed a shorter
sequence of only 257 base pairs (table 1). An
unrooted analysis of these data with transi-
tions and transversions weighted equally re-
sulted in two equally parsimonious trees, each
of which supported bat monophyly (Am-
merman and Hillis, 1992). Employing sev-
eral quantitative measures of confidence that
can be placed on a hypothesis in the context
of a particular data set (e.g., g, statistic, boot-
strapping, Templeton’s test, T-PTP), Am-
merman and Hillis (1992) demonstrated that
their phylogenetic results were statistically
significant. Additional rooted and unrooted
analyses including only transversion data also
supported bat monophyly (Ammerman and
Hillis, 1992). In the unrooted analyses, eight
or nine substitutions (six of which were unique
in the data set) separated bats from the other
mammals in the tree (Ammerman and Hillis,
1992).

1994

A third analysis of 12S rDNA data was
conducted by Springer and Kirsch (1993).
These authors analyzed a data set of 412 base
pairs in two bats and members of 13 other
mammalian orders (table 1). While this study
included more taxa and longer nucleotide se-
quences than that of Ammerman and Hillis
(1992), the goal of Springer and Kirsch’s study
was evaluation of paenungulate relation-
ships, not bat monophyly, and their taxo-
nomic sampling was limited with respect to
archontan mammals. Members of Dermop-
tera and Scandentia were not included in the
study, and the bat suborders were each rep-
resented by only a single species (Springer
and Kirsch, 1993). An analysis of the 12S
data including all substitutions (transver-
sions and transitions) resulted in a mono-
phyletic Chiroptera in each of four equally
parsimonious shortest trees (Springer and
Kirsch, 1993: fig. 2). However, some trees
only one step longer did not support bat
monophyly, and a bootstrap analysis could
not resolve the relationships of bats at a 50
percent level (Springer and Kirsch, 1993).
Another analysis based exclusively on trans-
version data failed to support bat monophy-
ly. Eptesicus (a microchiropteran) grouped
with a cetacean in all ten of the shortest trees,
and Macroglossus (a megachiropteran)
grouped with an edentate in nine of the ten
trees (Springer and Kirsch, 1993: fig. 4). Weak
support for bat monophyly was found in a
third analysis using Lake’s method of invar-
iants applied to a data set that included the
bats, a primate, and a marsupial + mono-
treme group (Springer and Kirsch, 1993).
Based on all of their analyses, Springer and
Kirsch (1993: 149) concluded that bat mono-
phyly received “‘mixed support’? in their
study. While it is clear that bat diphyly sensu
Pettigrew et al. (1989) was not supported in
any of Springer and Kirsch’s (1993) analyses,
there also seems to be little clear support for
bat monophyly. Especially given the small
number of bat species included in this study,
a more appropriate interpretation of the data
and results may be that they are inconclusive
with respct to the issue of bat monophyly.

Honeycutt and Adkins (1993) combined
sequences from three genes (COII, IRBP, and
e-globin) in a single, large data set. Bats and
members of five other mammalian orders

SIMMONS: CHIROPTERAN MONOPHYLY 13

were included in the study (table 1). Chirop-
teran monophyly was supported in an un-
rooted parsimony analysis based on all sub-
stitutions, and also in an alternative analysis
including only transversions (Honeycutt and
Adkins, 1993).

RESULTS OF MORPHOLOGICAL STUDIES

Numerous morphological studies have
been conducted in recent years, and the ma-
jority of these support bat monophyly (table
2). The data employed include features of
fetal membranes, wing musculature, postcra-
nial and cranial osteology, vascular system,
volume of brain components, and combi-
nations of these and other data. Only two
data subsets apparently support bat diphyly:
features of the nervous system (Pettigrew,
1986, 199la, 1991b; Pettigrew et al., 1989;
Johnson and Kirsch, 1993) and of the penis
(Smith and Madkour, 1980). The results of
relevant morphological studies of bat rela-
tionships are summarized below; putative
morphological synapomorphies of Chirop-
tera are discussed in a subsequent section.

Smith and Madkour (1980) investigated
structure of the penis in bats and members
of five other mammalian orders, and com-
bined the penis data with characters from
other anatomical systems in a phylogenetic
analysis. Smith and Madkour (1980) identi-
fied two derived features of the penis, two
brain characters, one dental character, and
one feature of the wrist that Megachiroptera
apparently shares with taxa other than Mi-
crochiroptera (i.e., Dermoptera, Primates,
and Scandentia). Lack of similarity of con-
ditions lumped together by Smith and Mad-
kour (1980: 360-361) has resulted in rejec-
tion of two of these putative synapomorphies,
“enlarged neocortex” and “‘derived, non-in-
sectivorous dentition” (Wible and Novacek,
1988; see also Henson, 1970; Campbell, 1980;
Koopman and MacIntyre, 1980). A third
character (“distal radius and lunar carpal
broadened’’) was discussed and rejected by
Wible and Novacek (1988) because the dis-
tribution and potential homologies of these
modifications were not as indicated by Smith
and Madkour (1980). The remaining char-
acters—two features of the penis and one brain

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16 AMERICAN MUSEUM NOVITATES

character— provide potential support for the
bat diphyly hypothesis.

In the late 1980s Pettigrew and his col-
leagues reported a series of derived features
of the nervous system that suggest that bats
are diphyletic (Pettigrew, 1986, 1991a, 1991b;
Pettigrew and Cooper, 1986; Pettigrew and
Jamieson, 1987; Pettigrew et al., 1989). Over
20 derived neural traits and one postcranial
character have thus far been cited by this
group in support of bat diphyly (see summary
in Pettigrew, 1991a). Details of several of the
characters employed in this study have been
questioned by various authors (e.g., Wible
and Novacek, 1988; Baker et al., 1991b; Sim-
monsetal., 1991; Thiele et al., 1991; Johnson
and Kirsch, 1993; Kaas and Preuss, 1993;
Simmons, 1993), but it seems clear that neu-
ral characters as a group strongly support bat
diphyly. This conclusion is also supported by
alternative analyses recently conducted by
Johnson and Kirsch (1993).

Johnson, Kirsch, and their colleagues are
responsible for a series of influential papers
entitled ““Phylogeny Through Brain Traits”
(Switzer et al., 1980; Johnson et al., 1982a,
1982b, 1984, in press; Kirsch, 1983; Kirsch
and Johnson, 1983; Kirsch et al., 1983). In
a reanalysis of data described in these pub-
lications, Johnson and Kirsch (1993) found
that their neural characters (many of which
differ from those employed by Pettigrew and
his colleagues) support bat diphyly. Addition
of five characters from Pettigrew’s data set
changed topology of the most parsimonious
tree somewhat, but diphyly of bats was still
supported when only neural characters where
considered in the analysis (Johnson and
Kirsch, 1993). However, when neural data
(29 characters) were combined with data from
other anatomical systems (65 characters from
Novacek et al., 1988), the results were strik-
ingly different—bats formed a monophyletic
group in the most parsimonious tree (John-
son and Kirsch, 1993). Specifics of the syn-
apomorphies supporting Chiroptera were not
discussed by these authors.

One additional study focusing on brain
morphology and bat phylogeny has been re-
ported but details of this work have not yet
been published. Lapoint and Baron (1993)
described in an abstract the results of mor-
phometric comparisons of volumes of 12

NO. 3103

brain components in bats and primates. Un-
specified methods were used to derive phy-
logenetic trees from these data, and statistical
methods were employed to compare these
trees with the monophyletic and diphyletic
models. According to Lapoint and Baron
(1993: 64), their “*. . . results corroborate the
monophyletic scenario in every situation .. .
The diphyletic model, on the other hand, was
found to be as likely as a random phylogeny
would be.’ However, these results must be
considered preliminary until a detailed ac-
count of this study has been published.

Luckett (1977, 1980a, 1980b, 1985, 1993)
extensively studied patterns of fetal mem-
brane formation in mammals and interpreted
these ontogenetic and morphological data in
a phylogenetic context. To evaluate bat re-
lationships, Luckett (1980b) developed a
character set of features of fetal membranes
and the forelimb, surveyed these characters
in extant archontan mammals (table 2), as-
sessed polarity by reference to numerous oth-
er mammalian orders, and conducted a man-
ual cladistic analysis of these data. Results of
this study indicate that bats are monophy-
letic; putative synapomorphies of Chiroptera
include four derived features of the forelimb
and two features of the fetal membranes
(Luckett, 1980b). Luckett (1993) subsequent-
ly conducted a revised analysis which in-
cluded data from fetal membranes and the
basicranium in archontans, rodents, and lag-
omorphs. Results of this new analysis simi-
larly supported chiropteran monophyly, and
three uniquely derived features of fetal mem-
branes were interpreted as synapomorphies
of bats (Luckett, 1993).

Wible and Novacek (1988) described sev-
eral new features of the skull and vascular
system of bats, reviewed the literature on bat
morphology and phylogeny, and summarized
data supporting bat monophyly. Their review
effectively considered all data relevant to the
bat monophyly controversy that had been
published as of 1987 (e.g., Luckett, 1980b;
Smith and Madkour, 1980; Calford et al.,
1985; Pettigrew, 1986; Pettigrew and Cooper,
1986). A total of 22 derived features sup-
porting bat monophyly were identified by
Wible and Novacek (1988: table 3), including
six cranial characters, nine osteological fea-
tures of the postcranium, three muscular

1994

characters, three features of the fetal mem-
branes, and one neural character. Although
the cranial characters were rejected by Pet-
tigrew et al. (1989: table 8), criticisms leveled
at these characters did not adequately address
issues of homology and the possibility of re-
versals within higher taxa (Baker et al., 199 1b;
Wible and Martin, 1993). Baker et al. (1991b)
published a tabular summary of the putative
bat synapomorphies reviewed by Wible and
Novacek (1988) and added five postcranial
features to the list. However, these additional
characters were not discussed further by Ba-
ker et al. (1991b) and they have never been
properly described or evaluated.

Thewissen and Babcock (1991, 1993) in-
vestigated morphology and innervation of the
propatagial muscle complex of bats and other
volant mammals (table 2). Wible and No-
vacek (1988) had listed “occipitopollicalis
muscle present on leading edge of propata-
gium’”’ as a synapomorphy of bats, but Pet-
tigrew et al. (1989) rejected this character on
the grounds that other volant mammals have
propatagial muscles as well. In 1991 Thewis-
sen and Babcock identified a uniquely de-
rived pattern of innervation in the propata-
gial muscle of bats (m. occipitopollicalis) that
suggests that presence of this muscle is indeed
a synapomorphy of Chiroptera. Expanding
their study to include additional taxa and
other features of the propatagium (table 2),
Thewissen and Babcock (1993) confirmed the
uniquely shared pattern of muscle innerva-
tion, and went on to identify two additional
features that indicate a single evolutionary
origin for the propatagial muscle in bats.
These data were interpreted as supporting
monophyly of Chiroptera (Thewissen and
Babcock, 1991, 1993).

In order to evaluate the phylogenetic re-
lationships of a variety of extinct archontans,
Beard (1993a) developed a data set of post-
cranial, cranial, and dental characters which
he surveyed in both extant and extinct forms
(table 2). An exhaustive parsimony analysis
of these data resulted in discovery of a single
most parsimonious tree in which Chiroptera
is monophyletic (Beard, 1993a). One unique
cranial and six postcranial characters were
identified as synapomorphies of bats (Beard,
1993a).

Szalay and Lucas (1993) also examined

SIMMONS: CHIROPTERAN MONOPHYLY 17

cranioskeletal features of fossil and living ar-
chontans, although they did not conduct an
explicit parsimony analysis of their data.
Based on various morphological compari-
sons, Szalay and Lucas (1993) concluded that
Chiroptera is monophyletic, and noted sev-
eral cranial and postcranial synapomorphies
of bats.

Wible and Martin (1993) examined the de-
velopment of the tympanic roof and floor in
a variety of archontan mammals, and devel-
oped a character set based on results of their
study (table 2). Although no explicit parsi-
mony analysis was conducted, they identified
two derived basicranial features that are
unique to bats, confirming some of the results
published earlier by Wible and Novacek
(1988).

Kay et al. (1992) conducted a cladistic
analysis of archontan mammals in order to
assess the affinities of the extinct paromo-
myid Jgnacius (table 2). For this purpose they
developed a set of 33 cranial characters which
could be scored in both extant and extinct
groups. The fossil form Asioryctes, a putative
primitive eutherian, was included as an out-
group to polarize characters (Kay et al., 1992).
A heuristic parsimony analysis of the com-
plete data set resulted in discovery ofa mono-
phyletic Chiroptera (Kay et al., 1992). A sec-
ond abbreviated data set was compiled by
assuming monophyly of Megachiroptera,
Microchiroptera, Primates, and Erinaceo-
morpha, and scoring each with the hypo-
thetical ancestral character states implied by
the initial heuristic analysis. Not surprisingly,
monophyly of bats was supported by ex-
haustive search analyses of this second data
set, and two unique cranial synapomorphies
of Chiroptera were identified. The shortest
“bat diphyly”’ tree sensu Pettigrew et al. (1989)
was found to be seven steps (17%) longer than
the most parsimonious tree (Kay et al., 1992).

Simmons (1993) summarized previously
published morphological character data from
most of the studies described above,? and
conducted a cladistic analysis of this inte-
grated data set (table 2). A total of 154 char-
acters in 6 subsets were included in Simmons’

2 Exceptions are a number of characters described for
the first time in Baker et al. (1991b), Kay et al. (1992),
and Wible and Martin (1993).

18 AMERICAN MUSEUM NOVITATES

(1993) study: cranial features excluding au-
ditory region (33 characters), auditory region
(20 characters), anterior axial skeleton and
forelimb (31 characters), hindlimb (35 char-
acters), reproductive tract and fetal mem-
branes (12 characters), and nervous system
(23 characters). These characters were scored
in seven extant taxa (Megachiroptera, Micro-
chiroptera, Galeopithecidae, Strepsirhini,
Tarsiiformes, Anthropoidea, Scandentia) and
three extinct taxa (Plesiadapidae, Par-
omomyidae, Micromomyidae); polarities
suggested by the original author(s) of the
characters were accepted for the purposes of
the study. The data thus collected were an-
alyzed under a variety of different assump-
tions, including different weighting systems,
different approaches to taxonomic polymor-
phism, inclusion and exclusion of fossils, etc.
Support for bat monophyly was found in ev-
ery analysis (Simmons, 1993). Although some
data subsets apparently support bat diphyly
(neural data), paraphyly (reproductive tract
+ fetal membranes), or are ambiguous (au-
ditory characters), the combined data set
clearly supports bat monophyly (Simmons,
1993). Simmons warned that the results of
this analysis should be considered prelimi-
nary because problems were detected with
the coding schemes and polarization criteria
applied to certain characters. However, sub-
sequent analyses of a corrected data set in-
cluding representatives of all of the mam-
malian orders have yielded the same
phylogenetic results (Simmons, in prep.). The
shortest “bat diphyly”’ trees are more than
20 steps longer than the most parsimonious
trees, all of which indicate monophyly of Chi-
roptera (Simmons, in prep.).

RESULTS OF STUDIES COMBINING
MORPHOLOGICAL AND MOLECULAR DATA

Only one study completed thus far has in-
cluded both morphological and molecular
data in single parsimony analysis (table 3).
Novacek (1994) combined morphological
data from previous studies (e.g., Luckett,
1980b; Novacek and Wyss, 1986; Novacek,
1986, 1990, 1992a; Wible and Novacek,
1988; Pettigrew et al., 1989; Thewissen and
Babcock, 1991) with nucleotide sequence data
from the COII gene (from Adkins and Hon-

NO. 3103

eycutt, 1991). A total of 49 morphological
characters plus variable sites from 684 base
pairs of nucleotide sequence were included
in the data set (Novacek, 1994). Unweighted
parsimony analysis of the entire data set (in-
cluding both transitions and transversions)
resulted in two equally parsimonious trees,
each of which supports monophyly of Chi-
roptera. A second analysis involving trans-
versions plus morphological characters (tran-
sitions omitted) produced a single most
parsimonious tree that similarly supports bat
monophyly (Novacek, 1994).

SUMMARY

The molecular and morphological studies
summarized above provide strong support
for chiropteran monophyly (tables 1, 2, 3).
Analyses of some molecular data sets have
yielded ambiguous results concerning bat re-
lationships (e.g., rDNA restriction sites, aA-
crystallin amino acid sequences, COI gene
sequences). However, analyses of most bio-
chemical and molecular data support mono-
phyly of Chiroptera (e.g., albumin immu-
nological distances, a-globin + 6-globin
amino acid sequences, nuclear e-globin and
IRBP gene sequences, mitochondrial 12S
rRNA and COII gene sequences). In no in-
stance have molecular data provided un-
ambiguous support for bat diphyly.

Morphological data show a slightly differ-
ent pattern (table 2). Neural and penial char-
acters generally support diphyly of bats, but
other data subsets clearly support bat mono-
phyly (e.g., characters of the cranium and
postcranial skeleton, vascular system, mus-
cles, and fetal membranes). Studies combin-
ing morphological data from many anatom-
ical systems strongly support bat monophyly
even when characters of the penis and ner-
vous system are included in the analysis
(Johnson and Kirsch, 1993; Simmons, 1993,
in prep.; Novacek, 1994). Chiropteran mono-
phyly is also supported when COII sequence
data and morphological characters are com-
bined in a single analysis (Novacek, 1994).

The most parsimonious interpretation of
the diverse morphological and molecular data
now available is that bats are monophyletic.
In this context, characters supporting bat di-
phyly should be interpreted as homoplastic.

1994

SIMMONS: CHIROPTERAN MONOPHYLY 19

TABLE 3
Analyses Combining Morphological and Molecular Data

Study Data

Novacek (1994) Diverse morphological
data + all substitutions
in COII gene nucleotide

sequences?

Diverse morphological
data + transversions in
COII sequences

Microchiroptera, Megachiroptera, Der-
moptera, Strepsirhini, Anthropoidea,
Artiodactyla, Rodentia, and
Edentata

Same as above

Taxa Conclusions

Bats monophyletic

Bats monophyletic

2 Data set included 49 morphological characters and information from 684 base pairs of the COII gene (see text
for data sources). The morphological data included 14 cranial characters, 22 postcranial characters, 3 characters of
the penis, 3 characters of the fetal membranes, and 7 neural characters.

Derived characters shared by megachirop-
terans and microchipterans represent poten-
tial synapomorphies of Chiroptera.

MORPHOLOGICAL CHARACTERS
SUPPORTING BAT MONOPHYLY

As discussed above, a large number of de-
rived morphological characters indicate that
Chiroptera is a monophyletic taxon. Unfor-
tunately, however, no adequate summary of
these features is available. Some putative
synapomorphies have been widely discussed
in the literature, but others have been cited
only in tabular summaries or have never been
noted in published discussions of bat mono-
phyly. In this section I describe those mor-
phological features that appear to be syn-
apomorphies of bats, review the taxonomic
distribution of each feature, and discuss ev-
idence for character polarity. Unreferenced
statements concerning osteological charac-
ters are based on my examination of speci-
mens in the collections of the AMNH (Amer-
ican Museum of Natural History, New York)
and the USNM (National Museum of Nat-
ural History, Smithsonian Institution, Wash-
ington, D.C.). Following Simmons (1993),
character dependence has been hypothesized
a priori only when two or more features of
possible ontogenetic and/or functional de-
pendence appear to have identical patterns
of taxonomic distribution. In cases where such
features do not have identical distributions,
they may represent independently evolving
structures and thus are described separately
below.

Interpretation of some characters may vary
depending on the phylogenetic placement of
Chiroptera within Eutheria. All of the fea-
tures listed below would be considered chi-
ropteran synapomorphies if bats nest within
Archonta with Dermoptera as their sister
group (sensu Novacek and Wyss, 1986; Wi-
ble and Novacek, 1988; Novacek, 1986, 1990,
1992a, in press; Johnson and Kirsch, 1993;
Szalay and Lucas, 1993; Simmons, 1993, in
prep.). Some characters, however, may be
considered ambiguous or plesiomorphic if
Archonta is not monophyletic and bats be-
long elsewhere in the mammalian family tree
(sensu Adkins and Honeycutt, 1991, 1993;
Stanhope et al., 1992, 1993). These aspects
of character interpretation are discussed sep-
arately for each character below.

DENTITION

Morphology of deciduous dentition. The
deciduous dentition of eutherian mammals
generally consists of incisors, canines, and
premolars, all of which are replaced by sec-
ond generation “adult” teeth during ontog-
eny. The form of the deciduous dentition is
typically similar to the adult dentition. De-
ciduous incisors, canines, and anterior pre-
molars resemble the teeth that will replace
them, and the posterior deciduous premolars
resemble adult molars in form. In all known
bats, however, the anterior deciduous den-
tition does not resemble the permanent den-
tition. The deciduous incisors, canines, and
first premolar are slender, projecting stylets
that are markedly recurved (fig. 1; Leche,
1875; Friant, 1963; Sigé, 1991). Each tooth

20 AMERICAN MUSEUM NOVITATES

has a long pedicle, and may be tipped with
as many as three sharp, curved cusps. This
pattern of deciduous dental morphology is
unique among mammals.

Living bats also differ from other mam-
mals in lacking molariform posterior decid-
uous premolars. However, some Eocene bats
apparently retained molariform deciduous
fourth premolars (Sigé, 1991). Because these
bats show affinities with living microchirop-
terans (Novacek, 1987; Habersetzer and
Storch, 1987, 1992; Sigé, 1991), it seems like-
ly that primitive microchiropterans—and the
most recent common ancestor of Megachi-
roptera and Microchiroptera—had molari-
form posterior deciduous premolars. Ab-
sence of these structures is derived within
Chiroptera and thus is not diagnostic of bats.

SKULL AND CRANIAL VASCULAR SYSTEM

Palatal process of premaxilla reduced; left
and right incisive foramina fused in midsa-
gittal plane. The majority of mammals have
a premaxilla with a well-developed palatal
process that is pierced by a pair of incisive
foramina on or near the premaxillary-max-
illary suture (Novacek, 1986; personal obs.).
A bar of bone derived from the premaxilla
extends along the midsagittal plane between
the right and left incisive foramina. This pre-
sumably represents the primitive condition
for mammals. In contrast, the palatal process
of the premaxilla is highly modified in most
bats (Dobson, 1875, 1878; Miller, 1907; An-
derson, 1912; Koopman, 1984, in press; Wi-
ble and Novacek, 1988).

In megachiropteran bats the palatal pro-
cess of the premaxilla is either lacking or is
reduced to a small element that supports the
incisor dentition but contributes little to the
palate itself (Anderson, 1912; Wible and No-
vacek, 1988). This morphology is associated
with fusion of the right and left incisive fo-
ramina to form a single opening just anterior
to the palatal processes of the maxillae (An-
derson, 1912; Wible and Novacek, 1988).

The palatal process of the premaxilla is also
reduced in microchiropteran bats, but mor-
phology of the anterior palate is quite vari-
able. In most microchiropteran families
the right and left incisive foramina are
not separated by a median bar of bone

NO. 3103

(e.g., Rhinopomatidae, Craseonycteridae,
Emballonuridae, Nycteridae, Megadermati-
dae, Natalidae, Thyropteridae, Vespertilion-
idae, and Molossidae). Exceptions include (1)
Phyllostomidae, in which the incisive foram-
ina are separated by a bar of bone connected
anteriorly with the facial processes of the pre-
maxillae; (2) some members of Mormoopi-
dae, which have incisive foramina separated
anteriorly by a very thin strut that may not
be ossified; (3) Myzopodidae, which have a
median bar of bone that is connected by a
pair of very thin bony struts to the facial
processes of the premaxillae, which do not
meet at the midline; (4) Rhinolophidae, which
have a median bar of bone but lack connec-
tions between this bar and the facial processes
of the maxillae (facial processes of premaxilla
absent); (5) some members of Mormoopidae,
in which the incisive foramina are apparently
reduced to tiny perforations (it is not clear if
these transmit nerves or only blood vessels);
and (6) Furipteridae, Mystacinidae, and Noc-
tilionidae, which lack patent incisive foram-
ina.

Consideration of the presumed relation-
ships among microchiropteran families (sen-
su Van Valen, 1979; Pierson, 1986; Griffiths
and Smith, 1991; Griffiths et al., 1992) sug-
gests that reduction of the palatal process of
the premaxilla and fusion of the incisive fo-
ramina are primitive for Microchiroptera and
Chiroptera. Separation of the incisive foram-
ina is a condition secondarily derived within
bats, apparently evolving independently in
phyllostomoids (1 and 2 above), myzopodids
(3), and rhinolophids (4). This interpretation
is supported by major differences in mor-
phology of the anterior palate in these three
groups (Dobson, 1875, 1878; Miller, 1907;
Anderson, 1912; Koopman, 1984, 1994). Re-
duction and loss of the incisive foramina (5
and 6 above) are other derived conditions
that apparently evolved well within Micro-
chiroptera.

Among eutherian mammals, fusion of the
incisive foramina is a derived condition that
is limited to bats, some hominoid primates
(Homo, Pongo), and sirenians (Kay et al.,
1992; Novacek, 1986; personal obs.). In si-
renians, the premaxillae are large and the pal-
atal process is not reduced (Domning, 1978),
suggesting that fusion of the incisive foram-

1994 SIMMONS: CHIROPTERAN MONOPHYLY 21

Fig. 1. Close-up views of the deciduous dentition of megachiropteran bats (A, B) and microchirop-
terans bats (C—F); see text for discussion. A. Pteropus gouldi (Pteropodidae, Pteropodinae; USNM
284137). B. Eonycteris spelaea (Pteropodidae, Macroglossinae; USNM 294809). C. Lasiurus cinereus
(Vespertilionidae; USNM 209475). D. Tadarida mexicana (Molossidae; USNM 147786). E. Thyroptera
discifera (Thyropteridae; USNM 143784). F. Carollia perspicillata (Phyllostomidae; AMNH 131770).

pub: AMERICAN MUSEUM NOVITATES

ina occurred independently in this taxon.
Relative reduction in the size of the fused
incisive foramina and consideration of the
presumed phylogenetic relationships among
primates (Martin, 1990) similarly suggest that
the condition in Homo and Pongo is not ho-
mologous with that seen in bats. Accordingly,
the condition seen in bats—fusion of the in-
cisive foramina and concomitant reduction
of the palatal process of the premaxilla—is a
plausible synapomorphy of Chiroptera.

Postpalatine torus absent. The postpala-
tine torus is a thick, rounded lip which forms
the posterior edge of the palate. This structure
is found in many eutherians including all non-
bat archontans (with the exception of Loris),
insectivorans, and the putative primitive pla-
cental Asioryctes (Kay et al., 1992). In con-
trast, all bats apparently lack a postpalatine
torus (Kay et al., 1992; personal obs.). The
posterior edge of the palate flares ventrally
in megachiropteran bats of the genus Epom-
ophorus, but the bone is thin and the lip is
not rounded (Anderson, 1912: fig. 36; per-
sonal obs.).

Novacek (1986: 83) suggested that “‘torus
weak or absent” is the primitive condition
for placental mammals. However, Kay et al.
(1992) interpreted this character differently.
As a convention in their analysis, Kay et al.
(1992: 488, 496) accepted the condition seen
in Asioryctes aS primitive for all characters
because this fossil taxon is believed to be
“close to the ancestry of all later placental
mammals.”’ Because Asioryctes has a post-
palatine torus, presence of this structure was
interpreted as the primitive condition by Kay
et al. (1992), and absence of a torus was con-
sidered to be relatively derived. If Chiroptera
nests within a clade that is characterized by
presence of a postpalatine torus (e.g., Ar-
chonta), this polarity assessment is probably
correct with respect to bats, and absence of
a torus would be parsimoniously interpreted
as a derived condition diagnosing Chirop-
tera. The primitive condition for Eutheria as
a whole remains ambiguous because mar-
supials and a variety of other orders lack a
postpalatine torus (Novacek, 1986).

Jugal reduced and jugolacrimal contact lost.
The jugal of most therian mammals is a rel-
atively large element that forms the antero-
ventral rim of the orbit and contacts the lac-

NO. 3103

rimal (Novacek, 1986; Wible and Novacek,
1988). This condition, which is seen in all
non-bat archontans, is apparently primitive
for Eutheria. In contrast, the jugal of bats is
arelatively small bone confined to the middle
of the zygomatic arch, separated from contact
with the lacrimal by the intervening zygo-
matic process of the maxilla (Wible and No-
vacek, 1988). Reduction in the extent of the
jugal and loss of a jugal-lacrimal contact is
seen even in those taxa which have a well-
developed postorbital process (e.g., Ptero-
pus).

Reduction of the jugal is clearly a condition
derived within mammals, but it is not limited
to bats. The jugal is reduced (and lacimal
contact lost) in erinaceomorphs, lagomorphs,
and some rodents (e.g., muroids), and the
jugal is entirely absent in pholidotans and
soricomorphs (Carleton and Musser, 1984;
Novacek, 1986; Wible and Novacek, 1988).
Based on the presumed phylogenetic rela-
tionships of these taxa (Miyamoto and Good-
man, 1986; Novacek, 1986, 1990, 1992a), it
seems quite likely that the jugal has been in-
dependently reduced in bats, lagomorphs,
pholidotans, and within Insectivora (Wible
and Novacek, 1988). If bats nest within a
clade characterized by an unreduced jugal
(e.g., Archonta), reduction of the jugal would
be parsimoniously interpreted as a synapo-
morphy of Chiroptera.

Two entotympanic elements in the floor of
the middle-ear cavity: a large caudal element,
and a small rostral element associated with
the internal carotid artery. Rostral and caudal
entotympanics are independent cartilages that
are found in the tympanic floor and roof of
many eutherian mammals (Klaauw, 1922;
MacPhee and Novacek, 1993; Wible and
Martin, 1993). MacPhee and Novacek (1993)
recently suggested that presence of at least
one such element may be primitive for Euth-
eria. Among eutherians, only bats, dermop-
terans, carnivorans, macroscelideans, and the
edentate Dasypus have both rostral and cau-
dal entotympanics (Klaauw, 1922; Reinbach,
1952; Hunt, 1974; MacPhee, 1981; Wible,
1984, 1993; Wible and Martin, 1993). Hy-
racoids have also been described as having
both elements (Klaauw, 1922; Wible and No-
vacek, 1988), but Fischer (1989) recently re-
ported that the caudal element is really a pro-

1994

cess of the petrosal. Of those taxa that possess
true rostral and caudal entotympanics, the
internal carotid artery runs in proximity to
the rostral element only in bats, dermopter-
ans, and carnivorans (Wible, 1993; Wible and
Martin, 1993). Of these forms, only bats and
carnivorans have a large caudal entotympan-
ic that forms in the posterior and postero-
medial walls of the tympanic floor (Wible and
Novacek, 1988; Wible, 1993; Wible and
Martin, 1993).

Bat and carnivorans share a similar pattern
of entotympanic morphology that includes a
large caudal entotympanic and a small rostral
entotympanic that is associated with the in-
ternal carotid artery (Wible, 1984; Hunt,
1974; Wible and Novacek, 1988; Wible and
Martin, 1993). Because entotympanics are
apparently absent in miacids (Matthew,
1909), the putative fossil sister group of Car-
nivora (Wyss and Flynn, 1993), it seems like-
ly that this entotympanic pattern evolved in-
dependently in bats and carnivorans (Wible
and Novacek, 1988). If so, this pattern would
be interpreted as a synapomorphy of bats.
However, if miacids actually had entotym-
panics similar to extant carnivorans (a pos-
sibility that cannot be ruled out given the
uncertainties of fossil preservation), and if
bats and carnivorans are closely related (a
possibility suggested by some molecular data),
then the entotympanic pattern described
above might apply at a higher taxonomic lev-
el and would not be considered a synapo-
morphy of bats.

Tegmen tympani tapers to an elongate pro-
cess that projects into the middle-ear cavity
medial to the epitympanic recess. The tegmen
tympani of bats is unique in that it is reduced
and tapers to an elongate process that projects
anteroventrally into the middle-ear cavity
(Wible and Novacek, 1988; Wible and Mar-
tin, 1993). This condition stands in contrast
to that seen in most other therians, in which
the tegmen tympani lacks an elongate pro-
jecting process and instead contributes ex-
tensively to the roof or wall of the epitym-
panic recess (Wible and Novacek, 1988; Wible
and Martin, 1993). Dermopterans resemble
bats in reduction of the tegmen tympani, but
the dermopteran tegmen tympani tapers to a
short rather than an elongate process (Wible
and Martin, 1993). The styliform tegmen

SIMMONS: CHIROPTERAN MONOPHYLY 23

tympani seen in bats is unique among mam-
mals and can thus be interpreted as a syna-
pomorphy of Chiroptera (Wible and Nova-
cek, 1988).

King (1991) studied fetal specimens of
Pteropus and claimed that megachiropterans
do not exhibit the chiropteran tegmen tym-
pani morphology described by Wible and
Novacek (1988). However, this argument was
refuted by Wible (1992), who demonstrated
that King had incorrectly identified the teg-
men tympani in skull sections (King’s “‘teg-
men tympani’”’ was actually the alisphenoid).
All bat species studied to date exhibit the
unique tegmen tympani structure described
above (Wible, 1992).

Proximal stapedial artery enters cranial
cavity medial to the tegmen tympani; ramus
inferior passes anteriorly dorsal to the tegmen
tympani. The majority of eutherians exhibit
a presumably primitive extracranial course
for the ramus inferior of the stapedial artery
(Wible, 1987, 1993; Wible and Novacek,
1988). This pattern involves origin of the ra-
mus inferior from the proximal stapedial ar-
tery within the middle ear space, and anterior
passage of the ramus inferior through the
middle ear ventral to the tegmen tympani
(Wible, 1987, 1993; Wible and Novacek,
1988). In contrast, bats, rodents, lagomorphs,
and macroscelideans exhibit an intracranial
course for this vessel (Wible, 1987, 1992; Wi-
ble and Novacek, 1988). In these taxa the
ramus inferior arises from the proximal sta-
pedial artery within the cranial cavity, and
then runs forward dorsal to the tegmen tym-
pani (Wible, 1987, 1992; Wible and Nova-
cek, 1988). The intracranial ramus inferior
of these taxa appears to be homologous to
the extracranial ramus inferior of other mam-
mals because both vessels are accompanied
by the lesser petrosal nerve (Wible, 1987,
1992; Wible and Novacek, 1988). King (1991)
indicated that megachiropterans lack the in-
tracranial pattern and instead exhibited the
extracranial course of the ramus inferior, but
Wible (1992) demonstrated that King was
misled by misidentification of the tegmen
tympani. Megachiropterans and microchi-
ropterans both exhibit a similar intracranial
course for this vessel (Wible and Novacek,
1988; Wible, 1992).

Prior to giving rise to the ramus inferior,

24 AMERICAN MUSEUM NOVITATES

the proximal stapedial artery enters the cra-
nial cavity rostral to or through the tegmen
tympani in rodents, lagomorphs, and mac-
roscelideans (Wible and Novacek, 1988). In
contrast, the proximal stapedial enters the
cranial cavity medial to the tegmen tympani
in all bats studied thus far (Wible and No-
vacek, 1988; Wible, 1992). This variation in
morphology suggests that the intracranial
course of the ramus inferior evolved inde-
pendently in bats and in a clade containing
rodents + lagomorphs + macroscelideans
(Novacek, 1986, 1990, 1992a; Wible and No-
vacek, 1988). The unique condition seen in
bats (proximal stapedial artery enters cranial
cavity medial to tegmen tympani; ramus in-
ferior has intracranial course) can thus be
considered a synapomorphy of Chiroptera.

POSTCRANIAL MUSCULOSKELETAL SYSTEM

Modification of orientation of scapular
spine and shape of scapular fossae; reduction
of height of spine; presence of a well-devel-
oped transverse scapular ligament. The ther-
ian scapula is characterized by presence of a
longitudinal scapular spine that separates two
areas of muscle attachment, the supraspinous
and infraspinous fossae. In most taxa the spine
originates opposite the midpoint of the gle-
noid fossa, and the axis of the scapular spine
lies either directly in line with the axis of
rotation of the head of humerus, or it is offset
only a few degrees (figs. 2, 3). This condition,
which is seen in marsupials, insectivorans,
and non-bat archontans, is presumably prim-
itive for eutherian mammals. In contrast, the
scapular spine in all bats originates at the
posterior edge of the glenoid fossa, and the
long axis of the spine is offset 20-—30° from
the axis of rotation of the humeral head (figs.
2, 3). This condition is apparently unique
among mammals.

The shift in orientation of the scapular spine
in bats is correlated with changes in the shapes
of fossae and the gross outline of the scapula
(fig. 3). Compared with that of other mam-
mals, the supraspinous fossa of bats has a
greatly reduced anterior border and an ex-
panded vertebral border. Because the scap-
ular spine is relatively short, the maximum
width of the infraspinous fossa occurs ap-
proximately midway along the fossa, in con-

NO. 3103

trast to other mammals in which this fossa
is widest at or near its distal end. Baker et al.
(1991b) suggested that reduction of the su-
praspinous fossa and enlargement of the in-
fraspinous fossa may be synapomorphic for
bats, but changes in fossa area have yet to be
demonstrated using morphometric tech-
niques. However, the suite of shape modifi-
cations described above, including reorien-
tation of the scapular spine, is unique to bats.

The scapular spine of most mammals is
relatively deep and corresponds in height to
the acromion process, with which it is con-
tinuous (fig. 2). As a result of their continuity,
the scapular spine effectively braces the acro-
mion process against forces transmitted
through the clavicle. Presence of a deep scap-
ular spine is presumably primitive for therian
mammals. In contrast, the scapular spine of
bats is reduced in height compared with the
condition described above (fig. 2; Strickler,
1978; personal obs.). Because the scapular
spine is low, the acromion process appears
to be more strongly arched and less well sup-
ported in bats than in other mammals (Baker
etal., 1991b). However, a well-developed lig-
amentous sheet known as the “transverse
scapular ligament”? spans the distance be-
tween the acromion process and the vertebral
border of the scapula in bats (Strickler, 1978:
40). This ligament effectively braces the acro-
mion process, apparently performing much
the same function as the scapular spine in
other mammals (Strickler, 1978; Altenbach,
1979). This arrangement is apparently unique
to bats.

All of the features described above involve
the scapular spine and are seen only in bats,
so it seems likely that they represent a single
character complex. This suite of modifica-
tions—reorientation of the scapular spine,
modification of the shape of the scapular fos-
sa, reduction in height of spine, and presence
of a well-developed transverse scapular lig-
ament—is an unambiguous synapomorphy
of Chiroptera.

Reduction of olecranon process and hu-
meral articular surface on ulna; presence of
ulnar patella; absence of olecranon fossa on
humerus. The elbow joint of bats is unique
among mammals in that the ulna has a small
olecranon process with a greatly reduced hu-
meral articular surface, and the humerus lacks
an olecranon fossa (Wible and Novacek, 1988;

1994 SIMMONS: CHIROPTERAN MONOPHYLY aS

Fig. 2. Two views of the right scapula of selected archontan mammals; see text for discussion. The
figures on the left provide an axillary view of the scapula with an oblique view of the glenoid fossa; the
glenoid fossa directly faces the viewer in the figures on the right. A. Tupaia glis (Scandentia; USNM
396664). B. Lepilemur mustelinus (Primates; AMNH 170557). C. Cynocephalus sp. (Dermoptera; AMNH
14021). D. Dobsonia crenulatum (Megachiroptera; USNM 543180). E. Vampyrum spectrum (Micro-
chiroptera;, AMNH 261379).

26 AMERICAN MUSEUM NOVITATES NO. 3103

“aggre

icm

Fig. 3. Dorsal view of the right scapula of selected archontan mammals; see text for discussion. A.
Tupaia glis (Scandentia; USNM 396664). B. Lepilemur mustelinus (Primates; AMNH 170557). C.
Cynocephalus sp. (Dermoptera; AMNH 14021). D. Dobsonia crenulatum (Megachiroptera; USNM
543180). E. Vampyrum spectrum (Microchiroptera, AMNH 261379).

Szalay and Lucas, 1993; personal obs.). All
living bats also apparently possess an “ulnar
patella,” an ossification in the tendon of m.
triceps that articulates with the humeral troch-
lea when the elbow is flexed, and rides over

the posterodistal surface of the humerus in a
shallow groove as the elbow is extended (Wal-
ton and Walton, 1970; Szalay and Lucas, 1993;
personal obs.). The shallow groove for the ul-
nar patella lies in the area occupied by the

1994

olecranon fossa in other mammals. The ulnar
patella, which is unique among mammals, is
apparently absent in some well-preserved fos-
sil Eocene microchiropterans (e.g., Jcaronyc-
teris, Jepsen, 1966; Szalay and Lucas, 1993).
Despite this observation, the singular mor-
phology of the ulnar patella suggests that this
element is homologous in megachiropterans
and microchiropterans and thus should have
been present in the common ancestor of bats.
Reduction of the olecranon process, reduction
of the humeral articular surface of the ulna,
loss of the olecranon fossa in the humerus,
and perhaps presence of an ulnar patella and
patellar groove characterize a unique suite of
elbow modifications that is a synapomorphy
of bats.

Extant cetaceans also exhibit reduction of
the olecranon process and loss of the olec-
ranon fossa. However, there is little reduction
in area of the humeroulnar articulation, and
reductions in the olecranon process and fossa
are correlated with lateral compression of the
long bones and development of a transverse
ridge on the humerus that restricts movement
in the anteroposterior plane (Barnes and
Mitchell, 1978; personal obs.). Early Tertiary
archaeocete whales retained a moderately
large olecranon process, and the elbow joint
was apparently capable of anteroposterior
movement (Kellogg, 1936; Barnes and
Mitchell, 1978). In this context, it seems most
likely that the elbow modifications seen in
cetaceans evolved independently of those seen
in bats. Morphology of the cetacean elbow
joint bears little resemblance to that seen in
bats, and there is no reason to believe that
bats and whales share any derived, homol-
ogous modifications of the elbow.

Absence of supinator ridge on humerus. The
supinator ridge is a thin, prominent ridge that
runs up the shaft of the humerus from the
lateral epicondyle, providing a wide surface
of origin for the supinator muscles of the fore-
arm (Flower, 1885). A supinator ridge was
present primitively in mammals and has been
retained in most noncursorial eutherian lin-
eages, including non-bat archontans (Flower,
1885; Wible and Novacek, 1988). In many
rodents and cursorial mammals the supinator
ridge is poorly developed, but the distal end
of the ridge is still visible at the lateral epi-
condyle. The supinator ridge is apparently

SIMMONS: CHIROPTERAN MONOPHYLY 27

entirely absent only in bats, cetaceans, lago-
morphs, and some rodents (e.g., Dasyprocta).
Consideration of the probable phylogenetic
relationships of these taxa (Miyamoto and
Goodman, 1986; Novacek, 1986, 1990,
1992a) suggests that absence of a supinator
ridge evolved independently in each of these
groups. In this context, absence of the supi-
nator ridge can be interpreted as a synapo-
morphy of bats.

Absence of entepicondylar foramen in hu-
merus. The entepicondylar foramen (=supra-
condylar foramen) is a foramen in the distal
humerus that communicates the median
nerve and brachial artery (Flower, 1885). Al-
though presence of this foramen appears to
be primitive for mammals, it is absent in a
variety of eutherian lineages. For example,
the entepicondylar foramen is present in most
insectivorans but absent in erinaceids, and is
present in many carnivorans but absent in
canids, ursids, and hyaenids (Flower, 1885).
Among archontan mammals, the entepicon-
dylar foramen is present in dermopterans,
lemuriformes, tarsiers, and most cebids, but
is absent in other anthropoids and scanden-
tians (Flower, 1885; personal obs.). The en-
tepicondylar foramen is uniformly absent in
bats (Wible and Novacek, 1988; personal
obs.). If bats are closely related to dermop-
terans and primates, absence of the foramen
may represent a synapomorphy of bats (Wi-
ble and Novacek, 1988). However, variabil-
ity of this feature within Eutheria suggests
that it may not be a particularly useful char-
acter at higher taxonomic levels.

Occipitopollicalis muscle and cephalic vein
present in leading edge of propatagium. Pro-
patagial muscles are present only in gliding
or flying mammals. In gliding squirrels and
dermopterans, the propatagial complex con-
sists of overlapping sheetlike muscles that ex-
tend from the side of the lower jaw to the
forearm and thumb (Thewissen and Babcock,
1991, 1993; Gray and Sokoloff, 1992). The
cephalic vein does not accompany the pro-
patagial muscles into the propatagium in these
taxa (Thewissen and Babcock, 1993). In con-
trast, the propatagial muscle in bats (m. oc-
cipitopollicalis) is a long, narrow muscle
which originates from the occipital region of
the skull and inserts on the base of the pollex
and second metacarpal. Tendinous or mus-

28 AMERICAN MUSEUM NOVITATES

cular slips may also originate on the face and
in the fascia covering the pectoral muscles,
and tendinous or elastic regions may inter-
vene between muscle bellies (Mori, 1960;
Stickler, 1978; Thewissen and Babcock, 1991,
1993). The cephalic vein accompanies m. oc-
cipitopollicalis into the propatagium in all
bats studied to date (Thewissen and Babcock,
1993).

Layers of the sheetlike propatagial muscles
in dermopterans are served by different
nerves, one receiving innervation from cra-
nial nerve VII (CN VII) and the other re-
ceiving innervation from cervical spinal
nerves (Thewissen and Babcock, 1991, 1993).
In contrast, individual muscle bellies in the
occipitopollicalis complex receive unusual
dual innervation from both CN VII and cer-
vical spinal nerves in at least two megachi-
ropterans (Pteropus and Haplonycteris) and
two microchiropterans (Myotis and Rhino-
poma; Thewissen and Babcock, 1991, 1993).
At least one microchiropteran (Tadarida)
lacks innervation from the cervical nerves,
but consideration of phylogenetic relation-
ships of the genera in question suggests that
this condition is derived within Microchi-
roptera (Thewissen and Babcock, 1991, 1993).
Dual innervation of the propatagial muscle
is apparently primitive for both Megachirop-
tera and Microchiroptera.

The propatagial muscle in flying squirrels
(Glaucomys) has recently been reported to
receive dual innervation like that of bats (Gray
and Sokoloff, 1992). However, Thewissen and
Babcock (1993) noted that in flying squirrels
the muscle slips innervated by CN VII are
restricted to the face and do not extend into
the propatagium. The dual innervation seen
in individual muscle bellies of m. occipito-
pollicalis is a pattern unique to bats (Thewis-
sen and Babcock, 1993). Dual innervation,
an occipital origin, and a close association
between m. occipitopollicalis and the ce-
phalic vein suggest that the propatagial mus-
cle complex of bats is uniquely derived within
mammals (Thewissen and Babcock, 1991,
1993). Presence of m. occipitopollicalis in the
propatagium (accompanied by the cephalic
vein) thus represents a synapomorphy of Chi-
roptera.

Digits II-V of forelimb elongated with com-
plex carpometacarpal and intermetacarpal

NO. 3103

joints, support enlarged interdigital flight
membranes (patagia); digits ITI- V lack claws.
The length of the digits of the hand (including
metacarpals and phalanges) are less than or
equal to the length of the forearm in most
mammals, including all cursorial forms. Each
digit in the hand is typically tipped with a
claw or homologous structure (nail or hoof).
The primitive condition for both the manus
and pes of mammals consists of five rela-
tively short, clawed digits with a phalangeal
formula of 2—3-3—3-3 (Flower, 1885; Carroll,
1988). This pattern is retained in edentates,
insectivorans, non-bat archontans, and most
other nonungulate eutherians (Flower, 1885;
personal obs.).

In contrast to other mammals, digits III-
V of bats (and sometimes digit II) are mark-
edly longer than the forearm, a specialization
that facilitates support of greatly enlarged in-
terdigital patagia (Wible and Novacek, 1988;
personal obs.). Elongation of the digits in bats
is accomplished through elongation of the
metacarpals and the proximal two phalanges.
The distal (third) phalanx on digits II-V is
often tiny or absent in chiropterans, although
the Eocene bat /caronycteris has a complete
phalangeal formula of 2—3—3-3-3 (Novacek,
1987). Claws are always absent on digits ITI-
V of bats, and are frequently absent on digit
II as well (Jepsen, 1966; Novacek, 1987; Wi-
ble and Novacek, 1988). Loss of claws and
elongation of the digits of the forelimb, as-
sociated with presence of large interdigital
patagia, represent a suite of forelimb modi-
fications that is unique to bats among mam-
mals.

Dermopterans, the only other mammals
that have interdigital patagia, have claws on
all digits of the manus and do not exhibit
marked elongation of the digits (Wible and
Novacek, 1988; personal obs.). In dermop-
terans the medial (second) phalanges are
elongated relative to the proximal (first) pha-
langes in digits II-V (Beard, 1990, 1993a),
but this modification falls far short of what
is seen 1n bats. Even if presence of interdigital
patagia is not a synapomorphy of bats (which
would be the case if Chiroptera and Der-
moptera are sister taxa), the relative propor-
tions of the digits and large size of the inter-
digital patagia are clearly unique to bats.

In most mammals, the proximal metacar-

1994

pals articulate with each other and with the
distal carpal elements in such a way as to
preclude complex movements of the meta-
carpals. Carpometacarpal joints are simple,
allowing only flexion and extension (Flower,
1885; personal obs.). Strong metacarpal lig-
aments bind the proximal metacarpals to one
another and hinder mediolateral (adduction/
abduction), rotative, and independent move-
ments of these elements. When present, fac-
ets associated with intermetacarpal joints are
simple and facilitate only limited flexion and
extension. This apparently represents the
primitive condition for mammals.

Bats are unique among mammals in having
complex carpometacarpal and intermetacar-
pal joints (Vaughan, 1959; personal obs.).
Each metacarpal has a unique set of proximal
facets for articulation with various convex
and concave surfaces on the distal carpals,
and metacarpals II-V have extensive com-
plex facets for articulation with one another
(Altenbach, 1979; personal obs.). This suite
of carpometacarpal and intermetacarpal ar-
ticulations permits extensive mediolateral
movements of the metacarpals (adduction/
abduction) but prevents anteroposterior
movements. These modifications apparently
brace the wing against the forces of the air-
stream and facilitate control of the shape and
camber of the interdigital patagia during flight
(Altenbach, 1979).

The suite of modifications described
above—elongations of the digits, loss of claws,
presence of interdigital patagia, and presence
of a highly derived complex of carpometa-
carpal and intermetacarpal articulations—is
unique to bats and therefore represents a syn-
apomorphy of Chiroptera. Cetaceans lack
claws and exhibit elongation of some digits
(usually II-III or I-IV), but digit elongation
is accomplished by addition of extra phalan-
ges to the digits rather than elongation of the
metacarpals and proximal phalanges, and
complex carpometacarpal and intermetacar-
pal articulations are lacking. There is no rea-
son to suspect that any of the forelimb mod-
ifications of cetaceans and bats are
homologous.

90° rotation of hindlimbs effected by reori-
entation of acetabulum and shaft of femur;
neck of femur reduced; ischium tilted dorso-
laterally; anterior pubes widely flared and pu-

SIMMONS: CHIROPTERAN MONOPHYLY 29

bic spine present; absence of m. obturator in-
ternus. The acetabulum in most mammals (in-
cluding monotremes and marsupials) is ori-
ented so that the axis of rotation of the femur
projects ventrolaterally from the hip (fig. 4C).
The shaft of the femur is markedly offset from
the femoral head and neck, which are in line
with the axis of rotation. The combined effect
assures that the shaft of the femur projects
ventrally and slightly laterally, keeping the knee
well below the level of the sacrum during most
normal movements.

In contrast to the typical mammalian pat-
tern, the femur of bats projects laterally and
slightly ventrally from the hip joint, and the
knee lies on or above the level of the sacrum
(fig. 4A, B). This represents an approximate
90° rotation in the orientation of the hind-
limb (Wible and Novacek, 1988). This effect
has been produced by a pair of major mod-
ifications: reorientation of the acetabulum to
face dorsolaterally rather than ventrolater-
ally, and reorientation of the shaft of the fe-
mur so that it lies approximately in line with
the axis of rotation of the hip joint (and the
head and neck of the femur) rather than being
markedly offset from this axis. These modi-
fications have been accompanied by other
changes, including a dorsolateral tilting of the
ischium, flaring of the anterior pubes (asso-
ciated with reorientation of the acetabulum),
and reduction in the neck of the femur (as-
sociated with reorientation of the shaft rel-
ative to the head of the femur). This suite of
modifications is unique among mammals.

M. obturator internus is a hip muscle which
originates from the inner surface of the ob-
turator membrane and the bony rim of the
obturator foramen, passes out of the pelvic
cavity dorsally, and then turns laterad to in-
sert on the greaeter trochanter of the femur.
This muscle is present in the majority of
mammals including marsupials, insectivo-
rans, and non-bat archontans, but it is absent
in all bats studied to date (Humphry, 1869;
Coues, 1872; MacAlister, 1872; Leche, 1886;
Le Gros Clark, 1924, 1926; Howell and
Straus, 1933; Reed, 1951; Vaughan, 1959,
1970b). Absence of m. obturator internus
seems to be functionally related to the pelvic
modifications noted above, as the tilting of
the ischium and flaring of the pubes have
apparently reoriented the site of origin of this

30 AMERICAN MUSEUM NOVITATES

Fig. 4. Posterior view of the right half of the
pelvis and articulated femur of two bats (A, B) and
a scansorial quadruped (C); see text for discussion.
A. Rousettus amplexicaudatus (Megachiroptera;
USNM 278616). B. Eumops perotis (Microchi-
roptera; AMNH 15751). C. Tupaia glis (Scanden-
tia; USNM 396664).

muscle so as to prevent effective function of
the muscle. If m. obturator internus had been
retained in bats, the muscle would have to
pass dorsomedially almost parallel to the sur-

NO. 3103

face of origin, and then negotiate an acute
lateral turn of at least 130° before inserting
on the femur. Modifications of the pelvis as-
sociated with reorientation of the hindlimb
may thus have precluded retention of this
muscle.

M. psoas minor is a pelvic muscle that orig-
inates on the lumbar vertebrae and inserts on
the anterior ramus of the pelvis. In most
mammals, this muscle inserts on a small pro-
jection known as the iliopectineal process,
which is typically located either on the ilium
or at the iliopubic junction (Coues, 1872;
Leche, 1886; Le Gros Clark, 1924, 1926;
Howell and Straus, 1933; Reed, 1951; per-
sonal obs.). In bats, however, the insertion
of m. psoas minor has shifted ventrally so
that it lies entirely on the pubis, well below
the level of the acetabulum (Humphry, 1869;
MacAlister, 1872; Vaughan, 1959, 1970b).
The projection on which the muscle inserts
has also become elongated to form a structure
known as the “‘pubic spine” (fig. 5; Vaughan,
1959; Szalay and Lucas, 1993). Some other
mammals (e.g., desman talpine insectivo-
rans) have an enlarged iliopectineal process,
but in no other group does m. psoas minor
insert on an elongated process of the pubis.
The change in location of insertion of m. psoas
minor (and development of a pubic spine) is
probably functionally associated with reori-
entation of the acetabulum and flaring of the
anterior pubes, conditions that are related to
the 90° rotation in position of the hindlimbs.

The morphological features described
above—90° rotation of hindlimbs effected by
reorientation of the acetabulum and shaft of
the femur, reduction of the neck of the femur,
dorsolateral tilting of the ischium, flaring of
the anterior pubes, presence of a pubic spine,
and absence of m. obturator internus—ap-
pear to be functionally related and thus seem
to represent a single character complex. This
complex is unique to bats among mammals.

Absence of m. gluteus minimus. This mus-
cle originates from the illium and inserts on
the greater trochanter of the femur, which it
abducts and rotates. M. gluteus minimus is
present in most mammals, including mono-
tremes, marsupials, and non-bat archontans
(Coues, 1872; Leche, 1886; Le Gros Clark,
1924, 1926; Howell and Straus, 1933; Ells-
worth, 1974). In contrast, m. gluteus mini-

1994

mus is absent in insectivorans and bats
(Humphry, 1869; MacAlister, 1872; Reed,
1951; Vaughan, 1959, 1970b). If bats nest
within a clade characterized by presence of
m. gluteus minimus (e.g., Archonta), absence
of this muscle may be interpreted as a syn-
apomorphy of bats. This would not be true
if bats are closely related to insectivorans.

It should be noted that absence of m. glu-
teus minimus may well represent another fea-
ture functionally linked with the suite of hip
modifications described above (i.e., those as-
sociated with reorientation of the hindlimb).
However, this cannot be assumed a priori
because absence of m. gluteus minimus, un-
like the other features, is not unique to bats.

Absence of m. sartorius. This muscle orig-
inates from the ilium and/or inguinal liga-
ment and inserts on the medial aspect of the
tibia. M. sartorius is present in monotremes,
marsupials, and most eutherians, including
erinaceid insectivorans and non-bat archon-
tans (Coues, 1872; Leche, 1886; Le Gros
Clark, 1924, 1926; Howell and Straus, 1933;
Reed, 1951; Ellsworth, 1974). Presence of this
muscle thus appears to be the primitive con-
dition for mammals.

M. sartorius is absent in bats, macrosce-
lideans, and soricid and talpid insectivorans
(Humphry, 1869; MacAlister, 1872; Leche,
1886; Reed, 1951; Vaughan, 1959, 1970b;
Wible and Novacek, 1988). Absence of this
muscle in some (but not all) insectivorans
suggests that m. sartorius has been lost within
insectivorans, and it has probably also been
lost independently in bats and macroscelid-
eans. If bats nest within a clade characterized
by presence of m. sartorius (e.g., Archonta),
then absence of this muscle would be inter-
preted as a synapomorphy of Chiroptera. This
might not be true if bats are closely related
to macroscelideans or insectivorans.

Vastus muscle complex not differentiated.
The vastus complex comprises a set of mus-
cles that originate on the proximal femur and
insert into the patella and patellar ligament.
These muscles apparently originate from a
single mass which differentiates into several
muscles during development. Five distinct
vastus muscles are seen in monotremes; three
are found in most eutherians (e.g., .insecti-
vorans, scandentians, primates), and two are
present in some taxa (e.g., marsupials,’ der-

SIMMONS: CHIROPTERAN MONOPHYLY 31

Fig. 5.
pelvis of a megachiropteran bat (A) and micro-
chiropteran bat (B); see text for discussion. Arrows
indicate the location of the pubic spine, the inser-
tion site of the psoas minor muscle. A. Dobsonia
crenulata (USNM 543180). B. Vampyrum spec-
trum (AMNH 261379).

Lateral view of the right side of the

mopterans; Coues, 1872; Leche, 1886; Le
Gros Clark, 1924, 1926; Howell and Straus,
1933; Reed, 1951; Ellsworth, 1974). In con-
trast, the vastus in bats consists of a single,
undifferentiated muscle mass (Humphry,
1869; MacAlister, 1872; Leche, 1886; Reed,
1951; Vaughan, 1959, 1970b). This unique
condition is apparently derived within mam-
mals.

Like other muscular modifications noted
above, lack of differentiation of the vastus
muscle complex may be functionally asso-
ciated with reorientation of the hindlimb.
However, this cannot be assumed a priori
because the number of differentiated muscles

In the vastus complex may have been reduced

in other mammalian groups (e.g., marsupials,
dermopterans) for reasons unrelated to hip
reorganization. Interpretation of transfor-
mations of this character in the basal branch-

32 AMERICAN MUSEUM NOVITATES

es of Mammalia is ambiguous, but it seems
clear that a completely undifferentiated vas-
tus is unique to bats.

Reorientation of upper ankle joint facets on
calcaneum and astragalus; trochlea of astrag-
alus convex, lacks medial and lateral guiding
ridges; tuber of calcaneum projects in plan-
tolateral direction away from ankle and foot;
peroneal process absent; sustentacular pro-
cess of calcaneum reduced, calcaneoastraga-
lar and sustentacular facets on calcaneum and
astragalus coalesced; absence of groove on as-
tragalus for tendon of m. flexor digitorum fi-
bularis. The upper ankle joint in mammals
is formed by a series of articulations between
the distal tibia and fibula and the astragalus
and calcaneum. Primitively, the eutherian
tibia articules with the astragalus, and the
fibula articulates with both the astragalus and
calcaneum (Szalay, 1977, 1984, 1993; Szalay
and Decker, 1974; Szalay and Drawhorn,
1980; Szalay and Lucas, 1993). The proximal
articular surfaces of the astragalus collective-
ly form an “astragalar trochlea,” which is typ-
ically saddle-shaped and bounded by medial
and lateral guiding ridges. The tibial and fib-
ular facets on the astragalar trochlea and on
the calcaneum lie in planes that are oblique
to the distal facets for the cuboid and navic-
ular, and the axis of the tuber of the calca-
neum (which projects in a posterior direction
away from the ankle and foot) passes through
the cuboid facet (Szalay, 1977, 1984, 1993;
Szalay and Decker, 1974; Szalay and Draw-
horn, 1980; Szalay and Lucas, 1993; personal
obs.). This arrangement constrains extension
at the upper ankle joint because the tuber of
the calcaneum limits movement of the tarsus
relative to the tibia and fibula.

Bats have a unique upper ankle joint which
permits almost full extension of the foot. The
trochlea of the astragalus lies in a plane par-
allel to that of the navicular facet. The troch-
lear surface is smoothly convex and lacks me-
dial and lateral guiding ridges (Wible and
Novacek, 1988; personal obs.). The fibular
facet on the calcaneum (when present) has
shifted its position to the lateral side of the
base of the calcaneal tuber, and in many forms
the plane of the fibular facet lies parallel to
that of the cuboid facet. The calcaneal tuber,
rather than projecting in a posterior direction
away from the foot, is directed plantolater-

NO. 3103

ally. As a result, the axis of the calcaneal tuber
no longer intersects the cuboid facet, but rath-
er passes through the anterior surface of the
body of the calcaneum. When the foot is ex-
tended, the calcaneal tuber does not interfere
with movement at the upper ankle joint. This
suite of modifications is unique to bats among
therian mammals.

The peroneal process of the calcaneum, un-
der which the tendon of m. peroneus longus
passes, projects laterally from the body of the
calcaneum in most mammals. The primitive
therian calcaneum was apparently character-
ized by a prominent peroneal process, but the
process has been reduced or lost in a variety
of lineages including bats, tupaiine scanden-
tians, and extant euprimates (Szalay, 1977,
1982, 1984; Szalay and Decker, 1974; No-
vacek, 1980; Szalay and Drawhorn, 1980;
Wible and Novacek, 1988; Szalay and Lucas,
1993). Because ptilocercine scandentians and
some Paleogene euprimates have a distinct
peroneal process, Wible and Novacek (1988)
suggested that this structure was lost inde-
pendently in bats, tupaiines, and within eu-
primates. Independent loss in bats seems par-
ticularly likely when reorientation of the
calcaneal tuber is taken into account. The
plantolateral orientation of the chiropteran
calcaneal tuber is unique, and this arrange-
ment effectively precludes presence of a pe-
roneal process (the normal location for the
mammalian peroneal process is occupied by
the base of the calcaneal tuber in bats).

The lower ankle joint of mammals com-
prises the joint between the calcaneum and
astragalus. Typically, two distinct points of
articulation are involved: a lateral calca-
neoastragalar articulation, and a medial sus-
tentacular articulation (Szalay and Decker,
1974; Szalay, 1977, 1982; Szalay and Lucas,
1993). The sustentacular facet on the calca-
neum is located on the sustentacular process,
a shelflike medial projection from the body
of the calcaneum; the calcaneoastragalar facet
is located on the body itself. The facets for
these two articulations are separate in mar-
supials, insectivorans, non-bat archontans,
and the majority of therian mammals (Szalay
and Decker, 1974; Szalay, 1977, 1982; Szalay
and Lucas, 1993; personal obs.). This pre-
sumably represents the primitive condition
for Theria.

1994

Bats are unique in that the sustentacular
process has been reduced and the calcaneoas-
tragalar and sustentacular facets are contin-
uous on the medial side of the body of the
calcaneum (Szalay and Lucas, 1993; personal
obs.). Wible and Novacek (1988: table 3) not-
ed that bats have the “calcaneal-astragalar
facet of the calcaneum modified from convex
process to depression or trough.” This ap-
pears to be a somewhat misleading descrip-
tion of the same modification: the “depres-
sion” or “trough” is actually formed by
coalescence of the two facets, which lie in
slightly different planes and form a concave
articular facet when fused. Similarly, Beard
(1993a) stated that the sustentacular facet is
greatly reduced or absent in bats, an impres-
sion that follows from identification of the
coalesced facets as the calcaneoastragalar fac-
et. Reduction of the sustentacular process
contributes to the impression that the sus-
tentacular facet is absent in bats.

M. flexor digitorum fibularis (=m. flexor
hallucis longus) originates from the postero-
distal surface of the fibula and the interos-
seous membrane, passes across the ankle me-
dial to the calcaneum, and inserts into the
ventral surfaces of the distal phalanges (Reed,
1951; Vaughan, 1959). There is a groove for
the tendon of this muscle on the posterior
surface of the astragalus in the majority of
mammals, including all non-bat archontans,
and presence of this groove is presumably
primitive for mammals (Beard, 1993a). Re-
arrangement of the upper and lower ankle
joints in bats has apparently resulted in a
somewhat different location for the tendon
of m. flexor digitorum fibularis. In bats, this
tendon apparently passes over the surface of
the calcaneum medial to the deflected cal-
caneal tuber (Vaughan, 1970b). Accordingly,
a groove for the tendon of m. flexor digitorum
fibularis is not present on the astragalus of
bats (Beard, 1993a), a condition that is ap-
parently unique to bats among therians.

The morphological features described
above—reorientation of upper ankle joint
facets on calcaneum and astragalus, a convex
astragalar trochlea lacking medial and lateral
guiding ridges, projection of the tuber of cal-
caneum in a plantolateral direction, absence
of the peroneal process, reduction of the sus-
tentacular process of calcaneum, coalescence

SIMMONS: CHIROPTERAN MONOPHYLY 33

of the calcaneoastragalar and sustentacular
facets on calcaneum and astragalus, and ab-
sence of groove on astragalus for tendon of
m. flexor digitorum fibularis—appear to be
functionally related and thus seem to repre-
sent a single character complex. This com-
plex is unique to bats among mammals.

Presence of calcar and depressor ossis styl-
iformes muscle. The calcar, a cartilaginous
and/or osseous element that extends from the
calcaneum to support the trailing edge of the
uropatagium, is a structure unique to bats.
M. depressor ossis styliformes, the muscle
that controls the position of the calcar rela-
tive to the tibia and ankle, is also unique. A
calcar is absent in one pteropodid (Sphaeri-
as), Craseonycteris, Rhinopoma, a few phyl-
lostomid species, and several Eocene micro-
chiropterans (including Jcaronycteris), but all
other bats (including Palaeochiropteryx) have
a calcar (Anderson, 1912; Jepsen, 1966; Wal-
ton and Walton, 1970; Smith, 1980; Haber-
setzer and Storch, 1987). Although m. de-
pressor ossis styliformes has been studied in
only a few taxa, it appears similar in mor-
phology in both megachiropterans and mi-
crochiropterans (Mori, 1960; Vaughan, 1959,
1970b; personal obs.). On the basis of pre-
sumed phylogenetic relationships among the
genera and families in question (Anderson,
1912; Van Valen, 1979; Smith, 1980; Pier-
son, 1986; Novacek, 1987), it seems likely
that the absence of the calcar and m. depres-
sor ossis styliformes in some bat taxa is a
secondarily derived condition. Presence of a
calcar and m. depressor ossis styliformes can
therefore be interpreted as a synapomorphy
of bats.

Shape of distal facet on entocuneiform. The
distal facet of the entocuneiform in most
mammals is very narrow and includes a strong
plantodistal process that interlocks with a
groove on the plantar surface of the first
metatarsal (Beard, 1993a). This presumably
represents the primitive condition for mam-
mals. In primates and dermopterans, the dis-
tal entocuneiform process is wide and the
plantodistal process is reduced or absent, a
condition that is relatively derived (Beard,
1993a). In contrast, bats have a proximodis-
tally shortened entocuneiform with a flat, tri-
angular distal facet (Beard, 1993a), a condi-
tion that is also derived with respect to the

34 AMERICAN MUSEUM NOVITATES

5mm

Fig. 6. Dorsal view of the foot of a megachi-
ropteran bat (A) and microchiropteran bat (B)
showing the relative proportions of the phalanges.
Note that the proximal phalanx of digit I (right
side of each figure) is greatly elongated relative to
those of the other digits. A. Rousettus amplexi-
caudatus (USNM 278616). B. Phyllostomus has-
tatus (AMNH 266071).

primitive mammalian pattern. Interpreta-
tion of the pattern of transformation of this
character depends upon perceived relation-
ships among bats, primates, and other mam-
malian orders. The chiropteran condition,
which is unique to bats among mammals,
may represent a synapomorphy of bats.
Elongation of proximal phalanx of digit I
of foot. The proximal phalanx of pedal digit
I-is less than or equal to the length of the
proximal phalanges of the other digits in non-
bat mammals. In contrast, the proximal pha-
lanx of digit I in most bats is approximately
1.5 times longer than the proximal phalanges

NO. 3103

of the othr pedal digits (fig. 7; Szalay and
Lucas, 1993; personal obs.). This elongation
effectively extends the length of digit I, which
has only two phalanges, and brings the claw
in line with those of the other pedal digits
(each of which have three phalanges). Elon-
gation of the proximal phalanx of digit I is
unique to bats among mammals.

Th proximal phalanx in digit I is not elon-
gated in three microchiropteran groups (Hip-
posiderinae, Thyropteridae, and Myzopodi-
dae). This difference is correlated with a
reduction of the number of phalanges in digits
II-V (Walton and Walton, 1970), another
condition that is clearly derived within mam-
mals. On the basis of presumed phylogenetic
relationships among the various families of
bats (Van Valen, 1979; Smith, 1980; Pierson,
1986; Novacek, 1987), it seems likely that
the ancestral condition for bats consisted of
a phalangeal formula of 2—3—3-3-3 with the
proximal phalanx of digit I elongated. By this
interpretation, secondary reduction of the
elongated first phalanx of digit I evolved con-
currently with reduction of the phalangeal
formula to 2—2—2—2-—2 in some microchirop-
teran lineages, thus preserving the ancestral
arrangement of the claws. Therefore, elon-
gation of the proximal phalanx of digit I
(which is seen in Megachiroptera and prim-
itively in Microchiroptera) can be interpreted
as a synapomorphy of bats.

FETAL MEMBRANES

Orientation of embryonic disc at time of
implantation. Implantation of the embryo in
the uterus generally occurs at the bilaminar
blastocyst stage of embryonic development.
At the time of implantation, the embryonic
disc typically exhibits one of three orienta-
tions relative to the mesentery of the uterus
(mesometrium). ‘“Mesometrial’ implanta-
tion describes a condition in which the em-
bryonic pole of the blastocyst is directed to-
ward the mesometrium; implantation is
termed “‘antimesometrial” when the abem-
bryonic pole is directed toward the meso-
metrium (Luckett, 1975, 1977, 1980b, 1993;
Mossman, 1987). “Orthomesometrial”’ ori-
entation describes a condition in which an
axis running through the embryonic and
abembryonic poles is oriented at a 90° angle

1994

to the mesometrium (Luckett, 1975, 1977,
1980b, 1993; Mossman, 1987). These pat-
terns of orientation remain constant through-
out early development in all non-bat placen-
tal mammals regardless of differences in the
degree of invasive activity that accompanies
implantation (Luckett, 1977, 1980b, 1993).

In megachiropterans and most microchi-
ropterans, the embryonic disc does not bear
a constant orientation to one pole of the uter-
us. Instead, the disc appears to be directed
toward the tubo-uterine junction rather than
bearing a specific orientation to the site of
mesometrial attachment (Rasweiler, 1979;
Luckett, 1980b, 1993). A few bats (vesper-
tilionids, thyropterids, desmodontines) ex-
hibit fixed antimesometrial implantation, but
this appears to be a condition derived within
Microchiroptera (Luckett, 1980, 1993). In this
context, orientation of the embryonic disc
toward the utero-tubal junction can be inter-
preted as a synapomorphy of Chiroptera
(Luckett, 1980b, 1993).

Differentiation of a free, glandlike yolk sac.
A free yolk sac forms early in development
and is maintained as a simple, sacciform
structure throughout most of gestation in the
majority of mammals, including most insec-
tivorans, dermopterans, and primates (Luck-
ett, 1975, 1977; Mossman, 1987). This con-
dition is presumed to be primitive for
mammals (Luckett, 1977). In megachirop-
terans and many microchiropterans (rhino-
pomatids, emballonurids, rhinolophids, mo-
lossids) a free yolk sac forms (fig. 7A, B, D)
but subsequently collapses to lie as a flattened
sac over the surface of the definitive placental
disc (Gopalakrishna, 1958; Luckett, 1980b,
1993; Rasweiler, 1990, 1992). The endoder-
mal cells of the yolk sac become hypertro-
phied, and the resulting yolk sac assumes a
unique “‘glandlike”’ appearance that is not seen
in other mammals (fig. 7C, E, F; Gopalak-
rishna, 1958; Luckett, 1977, 1980b, 1993;
Mossman, 1987; Wible and Novacek, 1988;
Rasweiler, 1990, 1992). This complex ap-
parently stores glycogen and lipids that serve
as an energy source just before parturition
(Stephans and Easterbrook, 1968; Rasweiler,
1990; Luckett, 1993). Presence of a free,
glandlike yolk sac is unique to bats among
mammals (Luckett, 1980b, 1993).

Microchiropterans that fail to develop as

SIMMONS: CHIROPTERAN MONOPHYLY 35

described above exhibit either of two derived
conditions: (1) paedomorphic retention of an
apparently absorptive bilaminar omphalo-
pleure (e.g., phyllostomids and noctilionids),
or (2) formation of a trilaminar omphalo-
pleure without development of a free yolk
sac, but with collapse and hypertrophy of the
yolk sac wall (e.g., megadermatids, thyrop-
terids, vespertilionids; Luckett, 1980b, 1993).
Both of these conditions appear to be derived
from a developmental pattern that involved
differentiation of a free, glandlike yolk sac
(Luckett, 1993). Because development of a
free, glandlike yolk sac appears to be primi-
tive for bats (and is unique to bats among
mammals), development of this structure can
be interpreted as a synapomorphy of Chi-
roptera.

Preplacenta and early chorioallantoic pla-
centa diffuse or horseshoe-shaped, with de-
finitive placenta reduced to a more localized
discoidal structure. The eutherian preplacen-
ta consists of a somewhat thickened layer of
trophoblast which forms where the maternal
epithelium of the uterus has broken down.
Maternal capillaries lie in close contact with
the trophoblast of the preplacenta, but no
fetal vessels have yet formed within the tro-
phoblast (Mossman, 1987). The preplacenta
eventually becomes vascularized on part or
all ofits fetal surface by the vascular allantois,
thereby establishing the definitive chorioal-
lantoic placenta (Luckett, 1980b; Mossman,
1987).

Placental development among bats is
unique in that it involves formation ofa broad
diffuse or horseshoe-shaped preplacenta and
early chorioallantoic placenta, which is later
reduced to form a more localized, discoidal
definitive placenta (fig. 7; Luckett, 1980b,
1993; Rasweiler, 1990, 1992). A broad dif-
fuse preplacenta also forms and is reduced in
hyracoids, but the definitive placenta is zo-
nary rather than discoidal (Mossman, 1987).
The pattern of early placental development
seen in bats occurs in no other group of mam-
mals and thus may be considered a synapo-
morphy of Chiroptera (Luckett, 1980b, 1993).

Definitive chorioallantoic placenta endo-
theliochorial. The degree of invasive activity
of the definitive chorioallantoic placenta var-
ies widely among mammals. Three major pla-
cental types are recognized. An “epitheli-

36 AMERICAN MUSEUM NOVITATES NO. 3103

Fig. 7. Stages in fetal membrane development in a megachiropteran bat (A—C) and microchiropteran
bat (D-F); see text for discussion. The developmental stages shown for the two bats are not equivalent,
but simply represent progressive stages in fetal development. The different stages in each sequence (e.g.,
A-C) have not been drawn to relative scale. A, B, C. Pteropus sp. (redrawn from Mossman, 1987: pl.
9). D, E, F. Molossus ater (redrawn from Rasweiler, 1992: figs. 18.6, 18.7, 18.9). A = allantois; CAP =
definitive chorioallantoic placenta; GYS = glandular yolk sac; PP = preplacenta; YS = yolk sac.

1994

ochorial’’ placenta is one in which there is no
loss of maternal tissue, so the chorionic tro-
phoblast is effectively separated from the ma-
ternal blood supply by at least two tissue lay-
ers (Luckett, 1977; Mossman, 1987). An
**endotheliochorial’’ placenta forms when the
maternal epithelium and all or part of the
underlying connective tissue are lost, result-
ing in apposition of the chorionic trophoblast
and the maternal capillary endothelium
(Luckett, 1977; Mossman, 1987). Finally, a
‘*hemochorial” placenta is established when
all of the maternal tissue separating the ma-
ternal blood from the trophoblast breaks
down, bathing the trophoblast in maternal
blood (Luckett, 1977; Mossman, 1987).

Two placenta types occur in bats: endothe-
liochorial and hemochorial. According to
Luckett (1980b: 257),

Maternal capillary endothelium persists within
the placenta and is separated from the syncy-
tiotrophoblast by a relatively thick, PAS-posi-
tive lamina (“interstitial membrane’’) in the
morphotype of the families Pteropodidae, Rhi-
nopomatidae, Rhinolophidae, Emballonuridae,
Megadermatidae, and Noctilionidae. Both com-
parative and ontogenetic analyses suggest that
this endotheliochorial relationship represents the
primitive chiropteran condition.

Some megachiropterans and members of the
remaining microchiropteran families devel-
op a hemochorial placenta, but this appears
to be a condition that is secondarily derived
within bats (Luckett, 1980b, 1993). Data from
an ultrastructural study of changing tissue re-
lationships during ontogeny of the placenta
in Myotis (Enders and Wimsatt, 1968) ap-
parently provide evidence for the transfor-
mation of endotheliochorial to hemochorial
placentation (Luckett, 1980b, 1993). In this
context, it seems most likely that the prim-
itive condition for bats is presence of an en-
dotheliochorial placenta (Luckett, 1980b,
1993).

Among non-bat eutherians, an endothelio-
chorial placenta is found in some edentates
(bradypodids), some insectivorans (soricids,
some talpids), tubulidentates, some rodents
(heteromyids), proboscideans, carnivorans,
scandentians, and two species of strepsirhine
primates (Luckett, 1975, 1977, 1980b, 1993;

SIMMONS: CHIROPTERAN MONOPHYLY 37

Mossman, 1937, 1987). Most strepsirhine
primates have an epitheliochorial placenta,
while other archontans (dermopterans, tar-
siers, and anthropoids) have a hemochorial
placenta (Luckett, 1975, 1977, 1980b, 1993;
Mossman, 1937, 1987). Although still the
source of some controversy (e.g., see Martin,
1990), it now appears that the epitheliochori-
al placenta is primitive for eutherian mam-
mals and probably for Archonta and Pri-
mates as well (Luckett, 1975, 1977, 1980b,
1993; Mossman, 1987).

Luckett (1975, 1977, 1993) has argued that
there is no uniform shared pattern of fetal
membrane development among most taxa
with an endotheliochorial placenta, and thus
that endotheliochorial placentation has
evolved convergently many times in mam-
mals. Luckett (1993: 175) observed that

... careful consideration of all developmental
features associated with endotheliochorial pla-
centation ..., including fate of the polar tro-
phoblast, amniogenesis, patterns of implanta-
tion, and fate of the definitive yolk sac, suggests
that an endotheliochorial placenta has devel-
oped homologously in the chiropteran subor-
ders, but convergently in carnivorans and scan-
dentians.

If bats are members of Archonta, then pres-
ence of an endotheliochorial placenta would
be interpreted as a synapomorphy of bats.
This feature was noted as a chiropteran syn-
apomorphy by Wible and Novacek (1988:
table 3), who described it as ‘“‘prominent ‘in-
terstitial membrane’ in the chorioallantoic
placenta.” It should be noted, however, that
some workers consider an endotheliochorial
placenta to be primitive for eutherian mam-
mals (e.g., Martin, 1990), while others do not
believe that bats belong to a monophyletic
Archonta (e.g., Stanhope et al., 1992, 1993).
Under these interpretations, endotheliocho-
rial placentation may be either ambiguous or
may represent a plesiomorphic condition.

NERVOUS SYSTEM

Cortical somatosensory representation of
forelimb reverse of that in other mammals.
Somatic sensory input from various parts of
the body is received by specific areas of the
neocortex in mammals. ““Somatotopic maps”

38 AMERICAN MUSEUM NOVITATES

of the primary somatosensory cortex (fig. 8)
may be obtained by systematically stimulat-
ing sensors in different parts of the body and
recording the pattern of electrical responses
in the neocortex. These maps typically con-
tain discrete representations of the body sur-
face. Somatotopic maps of primary somato-
sensory cortex reveal a similar orientation of
forelimb representation in most mammals,
with the distal elements of the forelimb oc-
curring rostral to more proximal elements in
the somatotopic map (fig. 8E). This relative
orientation of the forelimb representation is
seen in monotremes, marsupials, and all non-
bat taxa studied thus far (Bohringer and Rowe,
1977; Kaas, 1983; Wible and Novacek, 1988).

Somatotopic maps have been compiled for
only three bats. In one microchiropteran
(Macroderma) and one megachiropteran
(Pteropus), somatosensory forelimb repre-
sentations are the reverse of that of the body,
which maintains the same relative position
as seen in somatotopic maps of other mam-
mals (fig. 8C, D; Calford et al., 1985; Wise
et al., 1986). This arrangement is apparently
unique among mammals. Pettigrew et al.
(1989) stated that one microchiropteran (An-
trozous) lacks this reversal of the forelimb
representation, and cited Zook and Fowler
(1982) and Zook (personal commun.) as the
sources of this information. However, data
supporting this claim have never been pub-
lished. Contra Pettigrew et al. (1989), Zook
and Fowler’s (1982) publication, which is an
abstract, contains no mention of forelimb
orientation. Kaas (personal commun.) has
seen the summary diagrams of Zook and
Fowler, and reports that they show the same
forelimb orientation in Antrozous as seen in
other bats. Given the data currently avail-
able, it seems likely that reversal of the fore-
limb representation represents another syn-
apomorphy of bats.

REJECTED PUTATIVE
SYNAPOMORPHIES

Recognition of phylogenetic relationships
and identification of synapomorphies is an
iterative process, and disagreements con-
cerning conclusions are common. Systema-
tists are often faced with lists of putative syn-

NO. 3103

apomorphies that must be evaluated in terms
of the observational methods employed, cri-
teria for homology, perceived levels of with-
in- and among-taxon variation, and the phy-
logenetic context in which a given feature is
interpreted. There are numerous reasons why
a putative synapomorphy may be validly re-
jected.

Perhaps the most basic reason for rejecting
a synapomorphy is simple observational er-
ror, when taxa have been cited as having a
feature that they do not actually exhibit, or
lacking a feature that is clearly present. Pu-
tative synapomorphies in such cases may be
found to apply at higher or lower taxonomic
levels than originally reported, or they may
be rendered ambiguous when the observa-
tional data are corrected. This can also occur
when additional sampling indicates that a
distribution originally inferred for a character
(e.g., uniform presence in a given family or
order) is incorrect. In some cases, more de-
tailed sampling within groups may document
levels of within-group variation that meet or
exceed the amount of among-group variation
originally perceived. This variation may re-
sult in such ambiguity that evolutionary in-
terpretation of a character becomes impos-
sible, leading to rejection of the feature as a
phylogenetic character at the taxonomic level
under consideration.

Other reasons for rejecting putative syn-
apomorphies involve definition and homol-
ogy of the features in question. Some char-
acters have been defined in vague terms that
suggest but do not support a hypothesis of
homology (e.g., “derived, non-insectivorous
dentition” cited by Smith and Madkour,
1980). If further comparisons or develop-
mental data indicate that non-homologous
conditions have been lumped together under
such a description (as in this case; Koopman
and MacIntyre, 1980), the character may be
rejected on the grounds that it fails an initial
test of similarity, a prerequisite for homol-
ogy. Such character descriptions are, essen-
tially, too superficial to be phylogenetically
informative.

Finally, a critical component of character
interpretation is the phylogenetic context. The
position of a clade in the phylogenetic tree
may strongly affect hypotheses of synapo-
morphy. For example, a particular character

1994

SIMMONS: CHIROPTERAN MONOPHYLY

PLAGIO-
PATAGIUM

Ye
f
0)
ae:
\
Se ee

CAUDAL

FOYL

MEDIAL (7 ff Vfy

39

Fig. 8. Cortical representations of the body surface as determined from somatosensory mapping
experiments; see text for discussion. All of the figures shown here were redrawn from Wise et al. (1986).
A. Body surface “map” reconstructed from receptive field data collected from two specimens of the
microchiropteran bat Macroderma gigas. B. Approximate location of the body surface map (A) in the
brain of Macroderma gigas. C. Schematic representation (homunculus) of the body surface of Macro-
derma gigas. Compare this homunculus with the cortical map in figure A, from which it was derived.
D. Schematic representation of the body surface of a megachiropteran bat, Pteropus poliocephatus (from
Calford et al., 1985). E. Schematic representation of the body surface of a laboratory rat (from Kaas,

1983). Note that the digits of the forelimb are directed caudally in both bats (C, D), but are directed
rostrally in the rat (E).

40 AMERICAN MUSEUM NOVITATES

may appear to be a synapomorphy of bats if
they nest within Archonta, but may be in-
terpreted as plesiomorphic if bats fall else-
where in the mammalian family tree. When
homoplasy is evident in a character, the iden-
tity of successive sister taxa may greatly in-
fluence evolutionary interpretation. If a de-
rived state is present in a clade but absent in
at least two successive sister taxa, that con-
dition can be interpreted as a synapomorphy
of the clade in question even if the derived
state appears in other taxa in the tree. It is
not appropriate to reject a putative synapo-
morphy simply because a similar condition
appears in another taxon; the phylogenetic
relationships among outgroup taxa must be
considered.

Several characters previously cited as chi-
ropteran synapomorphies do not appear to
be valid under closer inspection, given the
assumptions of this study. Reasons for re-
jecting each putative synapomorphy are dis-
cussed below.

Ramus infraorbitalis of the stapedial artery
passes through the cranial cavity dorsal to
the alisphenoid. Wible and Novacek (1988)
cited an intracranial course of the ramus in-
fraorbitalis of the stapedial artery as a syn-
apomorphy of bats. The majority of euther-
ian mammals exhibit one of two extracranial
courses: passage through the orbitotemporal
region ventral to the alisphenoid, or passage
through a canal in the alisphenoid (Wible,
1987, 1993; Wible and Novacek, 1988). Based
on the distribution of these states, Wible
(1987, 1993) and Novacek (1986) argued that
passage ventral to the alisphenoid is primi-
tive for Eutheria. In contrast, in bats the ra-
mus infraorbitalis has an intracranial course
which passes through the orbitotemporal re-
gion dorsal to the alisphenoid (Wible and No-
vacek, 1988; Wible, 1993). This intracranial
vessel is apparently not homologous with the
extracranial ramus infraorbitalis of other
mammals because both vessels occur in some
microchiropterans (Buchanan and Arata,
1967; Wible and Novacek, 1988).

Kallen (1977) indicated that the intracra-
nial ramus infraorbitalis is absent in at least
two bat taxa, Rhinolophus (Rhinolophidae)
and Desmodus (Phyllostomidae). Wible and
Novacek (1988) interpreted this as a second-
arily derived condition because other rhinol-

NO. 3103

ophids and phyllostomids possess the intra-
cranial vessel. An intracranial vessel similar
to that seen in bats is present in some sori-
comorph insectivorans, but other sorico-
morphs and erinaceomorphs lack this vessel
(Roux, 1947). This distribution pattern led
Wible and Novacek (1988) to conclude that
an extracranial ramus infraorbitalis is prim-
itive for insectivorans. Accordingly, the in-
tracranial vessel seen in bats appears to be
independently derived, and presence of this
vessel was interpreted as a chiropteran syn-
apomorphy by Wible and Novacek (1988).

Recognition of the intracranial ramus in-
fraorbitalis as a synapomorphy of bats as-
sumes that this vessel is absent in the sister
taxa of bats. This appeared to be true at the
time of Wible and Novacek’s (1988) study,
but that is no longer the case: Wible (1993)
recently noted that an intercranial ramus in-
fraorbitalis is present in juvenile dermopter-
ans. If bats and dermopterans are sister taxa
as suggested by Novacek and Wyss (1986),
Wible and Novacek (1988), Novacek (1986,
1990, 1992a), Johnson and Kirsch (1993),
Szalay and Lucas (1993), Simmons (1993, in
prep.), and Wible (1993), then presence of an
intracranial ramus infraorbitalis cannot be
considered a synapomorphy of bats. Rather,
it apparently applies at a higher taxonomic
level—that of Volitantia (Dermoptera +
Bats).

Lesser tuberosity of humerus projects prox-
imally beyond the level of the articular sur-
face of the humeral head. The lesser tuber-
osity of the humerus is often called the
“trochin” in bats. Beard (1993a) indicated
that projection of this structure beyond the
level of the articular surface of the humeral
head is a synapomorphy of Chiroptera. This
condition stands in contrast to that seen in
most mammals, where the lesser tuberosity
of the humerus does not extend beyond the
level of the humeral head (Beard, 1993a; per-
sonal obs.).

While projection of the lesser tuberosity
beyond the humeral head is clearly derived,
Beard’s (1993a) interpretation of this feature
appears to be incorrect. The lesser tuberosity
does not extend beyond the articular surface
of the humeral head in many microchirop-
terans (e.g., Balantiopteryx, Thyroptera, Mo-
lossus; Smith, 1972: fig. 6) nor in any mega-

1994

chiropterans (Vaughan, 1970a: fig. 13;
personal obs.). Projection of the lesser tuber-
osity of the humerus beyond the head appears
to be a condition derived within Microchi-
roptera, and thus cannot be a synapomorphy
of bats.

90° rotation of manus. Wible and Novacek
(1988: table 3) listed ‘“‘manus rotated 90° from
position typical for quadrupedal mammals”
as a synapomorphy of bats. In quadrupedal
mammals the axis of flexion of the proximal
wrist joint lies roughly parallel to the axis of
flexion of the elbow during normal locomo-
tion. This presumably represents the primi-
tive condition for mammals. Morphology of
the wrist and elbow in cursorial mammals
precludes rotation of the manus, effectively
locking the axis of flexion of the manus into
the parallel position. In bats, similar modi-
fications of the elbow and reduction of the
distal ulna lock the manus into a fixed po-
sition relative to the elbow, but the axis of
flexion of the proximal wrist joint lies at an
angle approximately 90° to that of the elbow.
This modification is the result of relative
twisting of the distal end of the radius, which
has realigned the axis of the radiocarpal facets
so that it is perpendicular (rather than par-
allel) to the axis of flexion of the elbow. While
this is clearly a derived condition, it is not
unique to bats—dermopterans exhibit the
same modifications. If bats and dermopter-
ans are sister taxa, then this derived character
cannot be considered a synapomorphy of bats.
Rather, it apparently applies at a higher tax-
onomic level—that of Volitantia.

Absence of pisiform. Beard (1993a) stated
that the pisiform is absent in bats, and in-
terpreted this as a synapomorphy of Chirop-
tera. If the pisiform were absent, this inter-
pretation would be correct; however, the
pisiform is present in both microchiropteran
and megachiropteran bats (Dobson, 1878;
Vaughan, 1959, 1970a; Jepsen, 1966, 1970;
Altenbach, 1979; personal obs.). Although
concealed in dorsal views of the wrist, a ro-
bust, rodlike pisiform extends obliquely
across the posteroventral surface of the chi-
ropteran carpus, where it is tightly bound by
ligaments to the cuneiform, magnum, and
trapezium (Vaughan, 1959, 1970a; Alten-
bach, 1979: fig. 31; personal obs.). Allen
(1893) noted that the pisiform may be absent

SIMMONS: CHIROPTERAN MONOPHYLY 41

in pteropines and rhinolophines, but my ex-
amination of specimens suggests that the pi-
siform in these forms is present but may be
fused to the magnum. In this context, absence
of the pisiform cannot be considered a syn-
apomorphy of bats.

Dorsal ischia meet above vertebral axis.
Orientation of the pelvis such that the dorsal
ischia meet above the vertebral axis was list-
ed as a possible synapomorphy of bats by
Baker et al. (1991b: table 1). While this con-
dition is indeed seen in a few megachirop-
terans and microchiropterans, my examina-
tion of skeletal material indicates that it is
not found in the majority of taxa in either
suborder. When the derived condition is
present (e.g., in Pteropus), variation exists
even within species. For example, the dorsal
ischia meet above the axis of the vertebral
column in male Pteropus tonganus (e.g.,
USNM 546349), but not in females of the
same species (e.g., USNM 546347). Accord-
ingly, this character does not appear to rep-
resent a valid synapomorphy of bats.

Tliosacral fusion involving last lumbar ver-
tebra. Involvement of the last lumbar ver-
tebra in the iliosacral fusion was listed by
Baker et al. (1991b: table 1) as a possible
synapomorphy of bats. This character is
problematic from several perspectives. First,
the distinction between “sacral”’ and “‘lum-
bar” vertebrae is typically based on presence/
absence of participation in the joint between
the ilium and the vertebral column. In evo-
lutionary terms, a vertebra may be trans-
formed from a lumbar to a sacral vertebra by
establishment of a joint with the ilium and
fusion with the other sacral vertebrae. In some
cases it may be recognized as a homolog of
the last lumbar vertebrae of other taxa, but
such homologies are hard to establish when
vertebral counts are taxonomically variable.
In bats, the number of thoracic, lumbar, and
sacral vertebrae varies considerably among
species. For example, Walton and Walton
(1970: table 1) noted 11-14 thoracic verte-
brae, 4—6 lumbar vertebrae, and 3-6 sacral
vertebrae in different bat taxa. Unfortunate-
ly, the total number of vertebrae in the tho-
racic through sacral series also varies among
bats (from 19-24; Walton and Walton, 1970),
so evolutionary subtraction of vertebrae from
one part of the series (e.g., lumbar) does not

42 AMERICAN MUSEUM NOVITATES

necessarily mean that homologs of those ver-
tebrae have been added to another part of the
vertebral series (e.g., thoracic or sacral). This
makes it very difficult to assess homologies
of vertebra associated with the iliosacral fu-
sion.

Even if the character description in Baker
et al. (1991b) is interpreted as indicating that
the last lumbar can be recognized as such
(e.g., it forms a contact with the ilium but is
not yet fully fused to the sacral vertebrae),
there are still problems with this character.
Most importantly, in most megachiropterans
and microchiropterans there is no contact be-
tween the last lumbar vertebrae (sensu lato)
and the ilium. The first vertebra that artic-
ulates with the ilium is typically highly mod-
ified, with transverse processes that extend
the full length of the centrum and contact the
ilium along their entire length. The centrum
and transverse processes are completely fused
with those of the succeeding sacral vertebra,
suggesting that the first vertebra involved in
the iliosacral joint should be considered a
“‘true”’ sacral vertebra sensu Flower (1885).
In a few instances a case may be made for
incorporation of the last lumbar into the il-
iosacral fusion in a particular specimen, but
the evidence supporting this conclusion is
based on comparisons of sacral morphology
within the species, not among higher taxa. In
this context, inclusion of the last lumbar ver-
tebra in the iliosacral fusion does not appear
to be a valid synapomorphy of bats.

DISCUSSION AND CONCLUSIONS

The molecular and morphological data
currently available strongly support bat
monophyly. Although some characters are
difficult to interpret, a large number of pu-
tative chiropteran synapomorphies have been
proposed. For example, 39 derived substi-
tutions in the e-globin sequence, 22 derived
substitutions in the IRBP sequence, 8 derived
substitutions in the 12S rDNA sequence, and
7 derived substitutions in the COII sequence
apparently diagnose Chiroptera (Adkins and
Honeycutt, 1991, 1993; Ammerman and
Hillis, 1992; Bailey et al., 1992; Stanhope et
al., 1992, 1993). Over 25 morphological syn-
apomorphies—many of which consist of
complex suites of modifications—also diag-

NO. 3103

nose Chiroptera (table 4). The fact that these
features represent many different anatomical
systems (dentition, skull, cranial vasculature
system, postcranial musculoskeletal system,
fetal membranes, nervous system) further
strengthens the case for bat monophyly.

The degree of character support for Chi-
roptera compares favorably with perceived
support for other mammalian groups that are
generally agreed to be monophyletic. Theria,
Eutheria, Primates, Carnivora, Perissodac-
tyla, Sirenia, and Proboscidea are each di-
agnosed by 6-10 morphological synapomor-
phies, fewer than half the number of features
that diagnose Chiroptera (Novacek, 1990;
Beard, 1993a; Fischer and Tassy, 1993; Wyss
and Flynn, 1993). In the e-globin sequence,
over 30 derived substitutions diagnose Chi-
roptera, while only 4 such substitutions di-
agnose Primates (Bailey et al., 1992). Alter-
natively, Primates is diagnosed by 18
transversions in the COII data set, while Chi-
roptera and Artiodactyla are each diagnosed
by 6-7 transversions (Adkins and Honeycutt,
1993). While measurements of branch length
clearly depend on taxonomic sampling, tree
topology, and methods used to define char-
acters (see discussion below), comparisons of
relative character support nevertheless sug-
gest that Chiroptera is one of the better sup-
ported clades within Mammalia.

From the conclusion that bats are mono-
phyletic it follows that wings and powered
flight evolved only once in mammals. As dis-
cussed earlier, the oldest known fossil bats
are fully volant microchiropterans from the
Early Eocene; megachiropteran bats first ap-
pear in the fossil record in the Late Eocene
(Jepsen, 1966; Van Valen, 1979; Habersetzer
and Storch, 1987; Novacek, 1987; Ducrocq
etal., 1993). Given these dates, it seems likely
that flight evolved in the chiropteran lineage
sometime in the Paleocene or even the Late
Cretaceous, 58-70 million years ago. More
precise estimates will depend upon increased
resolution of the branching pattern of the var-
ious eutherian orders.

WHAT IS THE SISTER GROUP OF BATS?

Critical questions remain concerning the
place of bats within Eutheria. While most
workers now agree that bats are monophy-

1994

SIMMONS: CHIROPTERAN MONOPHYLY 43

TABLE 4
Morphological Synapomorphies of Chiroptera’

1) Deciduous dentition does not resemble adult den-
tition; deciduous teeth with long, sharp, recurved
cusps.

2) Palatal process of premaxilla reduced; left and right
incisive foramina fused in midsagittal plane.

3) Postpalatine torus absent.

4) Jugal reduced and jugolacrimal contact lost.

5) Two entotympanic elements in the floor of the mid-
dle-ear cavity: a large caudal element, and a small
rostral element associated with the internal carotid
artery.

6) Tegman tympani tapers to an elongate process that
projects into the middle-ear cavity medial to the
epitympanic recess.

7) Proximal stapedial artery enters cranial cavity me-

dial to the tegmen tympani; ramus inferior passes

anteriorly dorsal to the tegmen tympani.

Modification of scapula: reorientation of scapular

spine and modification of shape of scapular fossae;

reduction in height of spine; presence of a well-de-
veloped transverse scapular ligament.

Modification of elbow: reduction of olecranon pro-

cess and humeral articular surface on ulna; presence

of ulnar patella; absence of olecranon fossa on hu-
merus.

10) Absence of supinator ridge on humerus.

11) Absence of entepicondylar foramen in humerus.

12) Occipitopollicalis muscle and cephalic vein present
in leading edge of propatagium.

13) Digits II-V of forelimb elongated with complex car-
pometacarpal and intermetacarpal joints, support
enlarged interdigital flight membranes (patagia);
digits III-V lack claws.

8

Nw”

9

or

@ See text for discussion.

letic, there is no agreement concerning the
identity of the sister taxon of bats. Mono-
phyly of Archonta—a clade supposed to con-
tain bats, dermopterans, primates, scanden-
tians, and several fossil taxa—has been
supported by many studies based on mor-
phological data (e.g., Smith and Madkour,
1980; Novacek and Wyss, 1986; Novacek,
1986, 1990, 1992a, in press; Wible and No-
vacek, 1988; Greenwald, 1991; Johnson and
Kirsch, 1993; Szalay and Lucas, 1993) and
combined morphological and molecular data
(Novacek, 1994). However, archontan
monophyly has been rejected in other studies
based on analyses of biochemical, molecular,

14) Modification of hip joint: 90° rotation of hindlimbs
effected by reorientation of acetabulum and shaft of
femur; neck of femur reduced; ischium tilted dor-
solaterally; anterior pubes widely flared and pubic
spine present; absence of m. obturator internus.

15) Absence of m. gluteus minimus.

16) Absence of m. sartorius.

17) Vastus muscle complex not differentiated.

18) Modification of ankle joint: reorientation of upper
ankle joint facets on calcaneum and astragalus;
trochlea of astragalus convex, lacks medial and lat-
eral guiding ridges; tuber of calcaneum projects in
plantolateral direction away from ankle and foot;
peroneal process absent; sustentacular process of
calcaneum reduced, calcaneoastragalar and susten-
tacular facets on calcaneum and astragalus coa-
lesced; absence of groove on astragalus for tendon
of m. flexor digitorum fibularis.

19) Presence of calcar and depressor ossis styliformes
muscle.

20) Entocuneiform proximodistally shortened, with flat,
triangular distal facet.

21) Elongation of proximal phalanx of digit 1 of foot.

22) Embryonic disc oriented toward tubouterine junc-
tion at time of implantation.

23) Differentiation of a free, glandlike yolk sac.

24) Preplacenta and early chorioallantoic placenta dif-
fuse or horseshoe-shaped, with definitive placenta
reduced to a more localized discoidal structure.

25) Definitive chorioallantoic placenta endotheliocho-
rial.

26) Cortical somatosensory representation of forelimb
reverse of that in other mammals.

and at least one morphological data set (e.g.,
Cronin and Sarich, 1980; Miyamoto and
Goodman, 1986; Bailey et al., 1992; Kay et
al., 1992; Stanhope et al., 1992, 1993; Adkins
and Honeycutt, 1993; Honeycutt and Ad-
kins, 1993; Sarich, 1993). Numerous clades
of both archontan and non-archontan mam-
mals have been proposed as the sister group
of bats (table 5). In this context, it is very
difficult to establish just which morphologi-
cal features (or nucleotide substitutions) are
chiropteran synapomorphies. Many unique
characteristics of bats, such as morphology
of the deciduous dentition, would be consid-
ered synapomorphies under any hypothesis

44 AMERICAN MUSEUM NOVITATES

that accepts chiropteran monophyly. How-
ever, interpretation of other features varies
according to the identity of the sister group
of bats.3

One source of confusion concerning chi-
ropteran relationships has been uneven tax-
onomic sampling. Many relevant studies have
included only a few taxa, thus groups iden-
tified as the sister taxon of bats in some anal-
yses (e.g., Carnivora; Stanhope et al., 1992)
were not even considered in other studies (e.g.,
Adkins and Honeycutt, 1991, 1993; Am-
merman and Hillis, 1992; Bailey et al., 1992;
Kay et al., 1992). Those morphological stud-
ies that included data from all or most of the
mammalian orders have uniformly identified
Dermoptera as the sister group of bats (e.g.,
Novacek and Wyss, 1986; Novacek, 1986,
1990, 1992; Wible and Novacek, 1988;
Greenwald, 1991; Johnson and Kirsch, 1993).
In contrast, conclusive molecular studies with
comparable taxonomic sampling—all of
which have relied on protein amino acid se-
quence data—have identified the sister taxon
of bats as a larger clade including some com-
bination of Scandentia, Insectivora, Carniv-
ora, Pholidota, and Tubulidentata (Miya-
moto and Goodman, 1986; Stanhope et al.,
1993). Of particular importance is the fact
that Dermoptera was not included in any of
these studies.

Examination of branch lengths in trees
based on analyses of molecular data (e.g., Ad-
kins and Honeycutt, 1991, 1993; Stanhope
et al., 1992, 1993) and morphology (e.g., Wi-
ble and Novacek, 1988; Simmons, 1993) in-
dicates that only a few putative synapomor-
phies link bats with any other eutherian order.
It is clear that Megachiroptera and Micro-
chiroptera share far more synapomorphies

3 It should be noted that alternative hypotheses of sis-
ter-group relationships may increase perceived character
support for chiropteran monophyly. For example, in this
study I have tentatively accepted Dermoptera as the sis-
ter group of bats (see Morphological Characters Sup-
porting Bat Monophyly). Accordingly, derived morpho-
logical traits shared by dermopterans and bats have been
interpreted as synapomorphies of Volitantia, from which
it follows that they must be plesiomorphic for Chirop-
tera. If Dermoptera and Chiroptera are not sister taxa,
however, these features may have evolved independently
in the two lineages, and thus may be added to the list of
possible synapomorphies of Chiroptera.

NO. 3103

with each other than Chiroptera shares with
any of its putative sister taxa. How can we
account for this pattern, and also for the di-
versity of opinions concerning the identity of
the sister group of bats? Although there are
problems associated with any supposition of
clocklike evolutionary change (Scherer, 1990),
one explanation for the pattern of synapo-
morphies is that the temporal length of the
common ancestral lineage shared by bats and
their sister taxon was very short compared
to the subsequent period of divergence. An-
other possibility is that evolution occurred
unusually rapidly in the bat lineage subse-
quent to its separation from its sister lineage.
Neither of these hypotheses can be addressed
until the relationship of Chiroptera to other
mammalian clades has been resolved.

DIRECTIONS FOR FUTURE RESEARCH

Given the compelling evidence which now
supports monophyly of Chiroptera, it seems
clear that future studies of higher-level rela-
tionships of bats should concentrate on re-
solving the position of bats within Eutheria
(and relationships within the two bat sub-
orders) rather than continuing to focus on bat
monophyly. While data relevant to bat
monophyly will always be of interest, it is
time to move beyond this controversy to in-
vestigate evolutionary problems at other tax-
onomic levels.

Future studies directed toward resolving
the relationships of Chiroptera to other or-
ders should include several components. In-
creased taxonomic sampling in the context
of some data subsets may prove particularly
productive. Analyses of nucleotide sequence
data hold great promise, but few studies to
date have included representatives of more
than half of the extant orders. As demon-
strated by Adkins and Honeycutt’s (1991,
1993) analyses of COII sequence data, ad-
dition of a few taxa can significantly affect
the outcome of a study. Future research in-
volving broad sampling of mammalian or-
ders may be expected to reveal phylogenetic
patterns not seen in previous studies. How-
ever, use of single species as exemplars of
diverse orders should be avoided, as artifacts
of within-group variation may affect the out-
come of analyses of among-group relation-
ships.

1994 SIMMONS: CHIROPTERAN MONOPHYLY 45

TABLE 5
Proposed Sister Group of Chiroptera

Sister clade

Dermoptera

Study
Gregory (1910); Novacek and Wyss

Type of data
Morphological

(1986); Novacek (1986, 1990,
1992a); Wible and Novacek (1988);
Greenwald (1991); Johnson and
Kirsch (1993); Simmons (1993);
Szalay and Lucas (1993); Wible

(1993)
Novacek (1994) Morphological + mole-
cular?

Dermoptera + Primates Beard (1993a, 1993b) Morphological
Primates + Scandentia Kay et al. (1992) Morphological
Dermoptera + Primates + Scan- Ammerman and Hillis (1992) Molecular

dentia?
Dermoptera + Primates + Scan- Bailey et al. (1992) Molecular

dentia + Lagomorpha‘
Scandentia + Insectivora + Car- Miyamoto and Goodman (1986) Molecular¢

nivora + Pholidota4
Insectivora (excluding Erinaceus) Stanhope et al. (1993) Molecular”

+ Tubulidentata?
Insectivora + Carnivora? Stanhope et al. (1993) Molecular&
Carnivora Stanhope et al. (1992, 1993) Molecular”
Artiodactyla! Adkins and Honeycutt (1993) Molecular

@ The data set included 49 morphological characters and information from 684 base pairs of the COII gene. An
analysis including the morphological data plus all substitutions in the COII data could not resolve the sister group
of bats. Dermoptera was identified as the sister group in an analysis that included morphological data and COII

transversions only.

6 Archonta was assumed to be monophyletic in the analysis.
© The only other taxon included in this study was Artiodactyla, which was used as an outgroup.

4 Dermoptera was not included in the study.

€ Combined protein data set including amino acid sequence data from a- and 6-globins, myoglobins, lens aA
crystallins, fibrinopeptides, cytochrome c, and ribonucleases.

f Amino acid sequence data from a - and @-globins.

8 Combined protein data set including amino acid sequence data from a- and §-globins, myoglobins, lens aA
crystallins, fibrinopeptides, cytochrome c, ribonucleases, and embryonic a- and 6-globins.

A RBP data.

? The most parsimonious tree was rooted through an edentate; Carnivora and Insectivora were not included in the

study.

When multiple representatives of orders
are included in a study, it may be useful to
constrain some analyses to preserve ordinal
or subordinal monophyly to facilitate inves-
tigation of relationships among these groups.
Springer and Kirsch (1993) included several
artiodactyls, rodents, and bats in their study
in order to test monophyly of these orders,
but never ran constrained analyses to eval-

uate eutherian relationships in the context of
ordinal monophyly. This omission is unfor-
tunate since there is strong evidence from
other data sets that each of these groups is
monophyletic (Prothero et al., 1988; Honey-
cutt and Adkins, 1993; Luckett and Harten-
berger, 1993; Simmons, 1993, this paper).
The importance of fossils for understand-
ing higher-level relationships of mammals has

46 AMERICAN MUSEUM NOVITATES

been highlighted in several studies (e.g., Beard,
1990, 1993a; Novacek, 1990, 1992a, 1992b).
Although phylogenetic studies including ex-
tinct taxa are often plagued by missing data,
the information preserved in such taxa may
be crucial for understand relationships among
extant forms. Studies by Beard (1990, 1993a)
and Kay et al. (1992) have demonstrated that
extinct paromomyids and plesiadapids should
be considered in phylogenetic studies of ar-
chontan mammals.

A potentially productive method for re-
solving bat relationships may be to combine
various data subsets in a “total evidence”
approach (Kluge, 1989; Jones et al., 1993).
Different subsets of morphological characters
have been routinely combined in phyloge-
netic analyses relevant to bat relationships
(e.g., Luckett, 1980b, 1993; Smith and Mad-
kour, 1980; Wible and Novacek, 1988; John-
son and Kirsch, 1993; Simmons, 1993), but
most molecular studies have focused on only
a single gene or protein (e.g., Adkins and
Honeycutt, 1991, 1993; Ammerman and
Hillis, 1992; Bailey et al., 1992). Although
some workers have combined different sub-
sets of molecular data (e.g., Czelusniak et al.,
1990; Honeycutt and Adkins, 1993), taxo-
nomic sampling has been a problem because
different data subsets typically sample sig-
nificantly different sets of taxa. Only one at-
tempt has been made to combine morpho-
logical and molecular character data in a single
analysis (i.e., Novacek, 1994).

Studies combining molecular and morpho-
logical data are of particular interest when
different data sets produce significantly dif-
ferent phylogenies. Although there is some
concern that information may be lost when
data sets are combined, and that large mo-
lecular data sets may “swamp out” the signal
from smaller morphological data sets, pre-
liminary results of total evidence analyses
have been promising (e.g., Novacek, 1994).
Jones et al. (1993: 100) observed recently that

... arguments regarding conflicts between mo-
lecular and morphological data are overstated.
... Rather than increasing uncertainty in phy-
logenetic inference, we see total evidence as
maximizing descriptive and explanatory power.
As Moritz and Hillis (1990: 4) pointed out,
“studies that incorporate both molecular and
morphological data will provide much better

NO. 3103

descriptions and interpretations of biological di-
versity than those that focus on just one ap-
proach.”

Integrated studies that include morpholog-
ical data from many organ systems— and mo-
lecular data from many genes and proteins—
may hold the key to unraveling eutherian re-
lationships, including the positions of Chi-
roptera and Primates. Continuing efforts to
identify new character sets, fill sampling gaps,
and refine analytical methods should be en-
couraged in hope that future studies will re-
solve the persistent problems of mammalian
phylogeny.

ACKNOWLEDGMENTS

This study grew out of work that I began
as a Kalbfleisch-Hoffman Research Fellow at
the American Museum of Natural History in
1989-1991. M. Novacek and R. MacPhee
were instrumental in encouraging me to pur-
sue this line of enquiry, and I am grateful to
them for their support. Thanks also to T.
Griffiths, K. Koopman, M. Novacek, A. Pef-
fley, R. Van Den Bussche, R. Voss, P. Vrana,
and J. Wible for generously reading earlier
versions of this manuscript and offering many
helpful comments. P. Wynne provided the
illustrations, and I thank her for her expertise
and patience. The analysis of postcranial
characters and preparation of the manuscript
were supported by National Science Foun-
dation Grant BSR-9106868.

REFERENCES
Adkins, R. M., and R. L. Honeycutt

1991. Molecular phylogeny of the superorder
Archonta. Proc. Natl. Acad. Sci. U.S.A.
88: 10317-10321.

1993. A molecular examination of archontan

and chiropteran monophyly. Jn R. D.
E. MacPhee (ed.), Primates and their
relatives in phylogenetic perspective, pp.
227-249. Advances in primatology se-
ries. New York: Plenum Press.
Allen, H.
1893. A monograph of the bats of North
America. Bull. U.S. Natl. Mus. 43: 1-
198.
Altenbach, J. S.

1979. Locomotor morphology of the vampire

1994

bat, Desmodus rotundus. Am. Soc.
Mammal. Spec. Publ. 6: 1-137.
Ammerman, L. K., and D. M. Hillis

1992. A molecular test of bat relationships:
monophyly or diphyly? Syst. Biol. 41:
222-232.

Anderson, K.

1912. Catalogue of the Chiroptera in the col-
lection of the British Museum, second
edition, volume I: Megachiroptera.
Trustees of the British Museum, Lon-
don.

Bailey, W. J., J. L. Slightom, and M. Goodman

1992. Rejection of the “flying primate’ hy-
pothesis by phylogenetic evidence from
the e-globin gene. Science 256: 86-89.

Baker, R. J., R. L. Honeycutt, and R. A. Van Den

Bussche

199la. Examination of monophyly of bats: re-
striction map of the ribosomal DNA
cistron. In T. A. Griffiths and D. Klin-
gener (eds.), Contributions to mam-
malogy in honor of Karl F. Koopman.
Bull. Am. Mus. Nat. Hist. 206: 42-53.

Baker, R. J.. M. J. Novacek, and N. B. Simmons
1991b. On the monophyly of bats. Syst. Zool.
40: 216-231.
Barnes, L. G., and E. D. Mitchell

1978. Cetacea. In V. J. Maglio and H. B. S.
Cooke (eds.), Evolution of African
mammals, pp. 582-602. Cambridge,
MA: Harvard Univ. Press.

Beard, K. C.

1990. Gliding behavior and palaeoecology of
the alleged primate family Paromomyi-
dae (Mammalia, Dermoptera). Nature
345: 340-341.

1993a. Phylogenetic systematics of the Prima-
tomorpha, with special reference to
Dermoptera. Jn F. S. Szalay, M. J. No-
vacek, and M. C. McKenna (eds.),
Mammal phylogeny: placentals, pp.
129-150. Berlin: Springer-Verlag.

1993b. Origin and evolution of gliding in Early
Cenozoic Dermoptera (Mammalia, Pri-
matomorpha). In R. D. E. MacPhee
(ed.), Primates and their relatives in
phylogenetic perspective, pp. 63-90.
Advances in primatology series. New
York: Plenum Press.

Benton, M. J.

1990. Phylogeny of the major tetrapod groups:
morphological data and divergence
dates. J. Mol. Evol. 30: 409-424.

Blumenbach, J. F.

1779. Handbuch der Naturgeschicht.
Bohringer, R. C., and M. J. Rowe

1977. The organization of the sensory and

SIMMONS: CHIROPTERAN MONOPHYLY 47

motor areas of the cerebral cortex in the
platypus (Ornithorhynchus anatinus). J.
Comp. Neurol. 174: 1-14.

Buchanan, G. D., and A. A. Arata

1967. Cranial vasculature of a neotropical
fruit-eating bat, Artibeus lituratus. Anat.
Anz. 124: 314-325.

Buttery, R. G., J. R. Haight, and K. Bell

1990. Vascular and avascular retinae in mam-
mals: a funduscopic and fluorescein an-
giographic study. Brain Behav. Evol.
35(3): 156-175.

Calford, M. B., M. L. Graydon, M. F. Huerta, J.
L. Kaas, and J. D. Pettigrew
1985. A variant of the mammalian somato-

topic map in a bat. Nature 313: 477-
479.

Campbell, C. B. G.

1980. The nervous system of the Tupaiidae:
its bearing on phyletic relationships. Jn
W. P. Luckett (ed.), Comparative biol-
ogy and evolutionary relationships of
tree shrews, pp. 219-242. New York:
Plenum Press.

Carleton, M. D., and G. G. Musser

1984. Muroid rodents. Jn S. Anderson and J.
K. Jones (eds.), Orders and families of
recent mammals of the world, pp. 289—
379. New York: Wiley.

Carroll, R. L.

1988. Vertebrate paleontology and evolution.
New York: W. H. Freeman.

Coues, E.
1872. Osteology and myology of Didelphys

virginiana. Mem. Boston Soc. Nat. Hist.

2: 41-154.

Cronin, J. E., and V. M. Sarich
1980. Tupaiid and archontan phylogeny: the

macromolecular evidence. In W. P.
Luckett (ed.), Comparative biology and
evolutionary relationships of tree
shrews, pp. 293-312. New York: Ple-
num Press.

Czelusniak, J.,. M. Goodman, B. F. Koop, D. A.
Tagle, J. Shoshani, G. Braunitzer, T. K.
Kleinschmidt, W. W. de Jong, and G. Matsuda
1990. Perspectives from amino acid and nu-

cleotide sequences on cladistic relation-
ships among higher taxa of Eutheria. Jn
H. Genoways (ed.), Current mammal-
ogy 2: 545-572. New York: Plenum
Press.

Dal Piaz, G.

1937. I. Mammiferi dell’Oligocene veneto.
Archaeopteropus transiens. Mem. Inst.
Geol., Univ. Padova 11: 1-8.

de Jong, W. W., J. A. M. Leunissen, and G. J.

Wistow

48 AMERICAN MUSEUM NOVITATES

1993. Eye lens crystallins and the phylogeny
of placental orders: evidence for a mac-
roscelid-paenungulate clade? In F. S.

Szalay, M. J. Novacek, and M. C. Mc-

Kenna (eds.), Mammal phylogeny: pla- ©

centals, pp. 5-12. Berlin: Springer-Ver-
lag.
Dobson, G. E.

1875. Conspectus of the suborders, families
and genera of Chiroptera arranged ac-
cording to their natural affinities. Ann.
Mag. Nat. Hist., Ser. 4, 16: 345-357.
Catalogue of the Chiroptera in the col-
lection of the British Museum. London:
British Museum, 567 pp.

Domning, D. P.

1978. Sirenian evolution in the North Pacific.
Univ. California Publ. Geol. Sci. 118:
1-178.

Donoghue, M. J., J. A. Doyle, J. Gauthier, A. G.

Kluge, and T. Rowe

1989. The importance of fossils in phylogeny
reconstruction. Annu. Rev. Ecol. Syst.
20: 431-446.

Ducrocg, S., J.-J. Jaeger, and B. Sigé

1993. Late Eocene southern Asian record of a
megabat and its inferences on the mega-
bat phylogeny. Bat Res. News 33: 41-
42. [Dated 1992 but issued in 1993]

Duke-Endler, W. S.

1958. System of ophthalmology, Volume 1,
The eye in evolution. London: Henry
Kimpton.

Ellsworth, A. H. F.

1974. Reassessment of muscle homologies and
nomenclature in conservative am-
niotes, the echidna, Tachyglossus, the
opossum, Didelphis, and the tuatara,
Sphenodon. Part 1: pelvic musculature.
Huntington, NY: Robert E. Krieger.

Enders, A. C., and W. A. Wimsatt

1968. Formation and structure of the hemo-
dichorial chorioallantoic placenta of the
bat (Myotis lucifugus lucifugus). Am. J.
Anat. 122: 453-490.

Felsenstein, J.

1984. Distance methods for inferring phylog-
enies: a justification. Evolution 38: 16-
24.

Fischer, M. S.

1989. Zur Ontogenese der Tympanalregion der
Procaviidae (Mammalia: Hyracoidea).
Gegenbaurs Morphol. Jahrb. 135: 795-
840.

Fischer, M. S., and P. Tassy

1993. The interrelation between Proboscidea,
Sirenia, Hyracoidea, and Mesaxonia: the
morphological evidence. Jn F. S. Szalay,

1878.

NO. 3103

M. J. Novacek, and M. C. McKenna

(eds.), Mammal phylogeny: placentals,

pp. 217-234. Berlin: Springer-Verlag.
Fleischer, G.

1973. Studien am Skelett des GehGrorgans der
Saugetiere, einschlieBlich des Men-
schen. Séugk. Mitt. (Munchen) 21:
1131-1239.

1978. Evolutionary principles of the mam-
malian middle ear. Adv. Anat. Em-
bryol. Cell Biol. 55: 5-67.

Flower, W. H.

1885. An introduction to the osteology of the
Mammalia, 3rd ed. London: MacMil-
lan.

Friant, M.

1963. Recherches sur la formule et la mor-

phologie des dents temporaires des Chi-
roptéres. Acta Anat. 52: 90-101.
Fritsch, G.

1911. Contributions to the histology of the

Pteropus eye. Z. Zool. 98: 288.
Gauthier, J., A. G. Kluge, and T. Rowe.

1988. Amniote phylogeny and the importance

of fossils. Cladistics 4: 105-209.
Gopalakrishna, A.

1958. Foetal membranes in some Indian Mi-
crochiroptera. J. Morphol. 102: 157-
197.

Gray, J. A., and A. J. Sokoloff

1992. Propatagial innervation in the flying
squirrel Glaucomys volans. Am. Zool.
32: 157A,

Greenwald, N. S.

1990. Cladistic analysis of chiropteran rela-
tionships: why megachiropterans are not
primates. Bat Res. News 31: 79-80.

1991. Primate-bat relationships and cladistic

analysis of morphological data. Am. J.
Phys. Anthropol., Supp. 12: 82.
Gregory, W. K.
1910. The orders of mammals. Bull. Am. Mus.
Nat. Hist. 27: 1-524.
Griffiths, T. A., and A. L. Smith
1991. Systematics of emballonuroid bats
(Chiroptera: Emballonuridae and Rhi-
nopomatidae), based on hyoid mor-
phology. Bull. Am. Mus. Nat. Hist. 206:
62-83.
Griffiths, T. A., A. Truckenbrod, and P. J. Spon-
holtz
1992. Systematics of megadermatid bats (Chi-
roptera, Megadermatidae), based on hy-
oid morphology. Am. Mus. Novitates
3031: 21 pp.
Groves, C. P.
1993. Order Primates. Jn D. E. Wilson and D.
M. Reeder (eds.), Mammal species of

1994

the world, a taxonomic and geographic
reference, 2nd ed., pp. 243-277. Wash-
ington, DC: Smithsonian Institution
Press.
Habersetzer, J., and G. Storch
1987. Klassifikation und funtionelle Fligel-
morphologie palaogener Fledermause
(Mammalia, Chiroptera). Cour For-
schungsinst. Senckenb. 91: 117-150.
Cochlea size in extant Chiroptera and
Middle Eocene microchiropterans from
Messel. Naturwissenschaften 79: 462-
466.
Henson, O. W.
1970. The central nervous system. Jn W. A.
Wimsatt (ed.), Biology of bats 2: 57-
152. New York: Academic Press.
Hill, J. E., and J. D. Smith
1984. Bats: a natural history. Austin, TX:
Univ. Texas Press.
Honeycutt, R. L., and R. M. Adkins
1993. Higher level systematics of eutherian
mammals: an assessment of molecular
characters and phylogenetic hypothe-
ses. Annu. Rev. Ecol. Syst. 24: 279-306.
Howell, A. B., and W. L. Straus
1933. The muscular system. Jn C.G. Hartman
and W. L. Straus (eds.), Anatomy of the
Rhesus monkey (Macaca mulatta), pp.
89-175. New York: Hafner.
Humphry, G. M.
1869. The myology of the limbs of Preropus.
J. Anat. Physiol. 3: 294-319.
Hunt, R. M.
1974. The auditory bulla in Carnivora: an an-
atomical basis for reappraisal of carni-
vore evolution. J. Morphol. 143: 21-76.
Jepsen, G. L.
1966. Early Eocene bat from Wyoming. Sci-
ence 154: 1333-1339.
Bat origins and evolution. In W. A.
Wimsatt (ed.), Biology of bats 2: 1-64.
New York: Academic Press.
Johnson, J. I., and J. A. W. Kirsch
1993. Phylogeny through brain traits: inter-
ordinal relationships among mammals
including Primates and Chiroptera. In
R. D. E. MacPhee (ed.), Primates and
their relatives in phylogenetic perspec-
tive, pp. 293-331. Advances in prima-
tology series. New York: Plenum Press.
Johnson, J. I., J. A. W. Kirsch, and R. C. Switzer
1982a. Phylogeny through brain traits: fifteen
characters adumbrate mammalian ge-
nealogy. Brain Behav. Evol. 20: 72-83.
Johnson, J. I., R. C. Switzer, and J. A. W. Kirsch
1982b. Phylogeny through brain traits: the dis-
tribution of categorizing characters in

1992.

1970.

SIMMONS: CHIROPTERAN MONOPHYLY 49

contemporary mammals. Brain Behav.
Evol. 20: 97-117.
Johnson, J. 1., J. A. W. Kirsch, and R. C. Switzer
1984. Phylogeny through brain traits: evolu-
tion of neural characters. Brain Behav.
Evol. 24: 169-176.
Johnson, J. I., J. A. W. Kirsch, R. L. Reep, and
R. C. Switzer
In press. Phylogeny through brain traits: more
character for the analysis of mammalian
evolution. Brain Behav. Evol.
Jones, J. K., and H. H. Genoways
1970. Chiropteran systematics. Jn R. H.
Slaughter and D. W. Walton (eds.),
About bats: a chiropteran symposium,
pp. 3-21. Dallas, TX: Southern Meth-
odist Univ. Press.
Jones, T. R., A. G. Kluge, and A. J. Wolf

1993. When theories and methodologies clash:
a phylogenetic reanalysis of the North
American ambystomatid salamanders
(Caudata: Ambystomatidae). Syst. Biol.
42: 92-102.
Kaas, J. H.

1983. What, if anything, is SI? Organization
of the first somatosensory area of the
cortex. Physiol. Rev. 63: 206-231.
Kaas, J. H., and T. M. Preuss
1993. Archontan affinities as reflected in the
visual system. Jn F. S. Szalay, M. J. No-
vacek, and M. C. McKenna (eds.),
Mammal phylogeny: placentals, pp.
115-128. Berlin: Springer-Verlag.
Kallen, F. C.
1977. The cardiovascular system. In W. A.
Wimsatt (ed.), Biology of bats 3: 289-
483. New York: Academic Press.
Kay, R. F., J. G. M. Thewissen, and A. D. Yoder
1992. Cranial anatomy of Jgnacius graybul-
lianus and the affinities of the Plesiad-
apiformes. Am. J. Phys. Anthropol. 89:
477—498.
Kellogg, R.
1936. A review of the Archaeoceti. Carnegie
Inst. Washington Publ. 482: 1-366.
Kilpatrick, C. W., and P. E. Nunez

1993. Monophyly of bats inferred from DNA-
DNA hybridization. Bat Res. News 33:
62. [Dated 1992 but not issued until
1993]
King, A. J.
1991. Re-examination of the basicranial anat-

omy of the Megachiroptera. Acta Anat.
140: 313-318.
Kirsch, J. A. W.
1983. Phylogeny through brain traits: objec-
tives and method. Brain Behav. Evol.
22: 53-59.

50 AMERICAN MUSEUM NOVITATES

Kirsch, J. A. W., and J. I. Johnson
1983. Phylogeny through brain traits: trees
generated by neural characters. Brain
Behav. Evol. 22: 60-68.
Kirsch, J. A. W., J. I. Johnson, and R. C. Switzer
1983. Phylogeny through brain traits: the
mammalian family tree. Brain Behav.
Evol. 22: 70-74.
Klaauw, C. J. van der

1922. Uber die Entwickelung des Entotym-
panicums. Tijdschr. Ned. Dierkd. Ver.
18: 135-174.
Kluge, A. G.
1989. A concern for evidence and a phyloge-

netic hypothesis of relationships among
Epicrates (Boidae, Serpentes). Syst. Zool.
38: 7-25.

Knight, A., and D. P. Mindell

1993. Substitution bias, weighting of DNA se-
quence evolution, and the phylogenetic
position of Fea’s viper. Syst. Biol. 42:
18-31.
Kolmer, W.

1910. Contribution to the study of the eye of
a macrochiropteran. Centralbl. Physiol.
23: 6.
The problem of the anatomy of the eye
of macrochiroptera. Z. Wiss. Zool. 97:
91.
1926. On the eye of the bat. Verh. Zool. Bot.
Ges. Wien 74: 29-31.
Koopman, K. F.
1984. A synopsis of the families of bats, Part
VII. Bat Res. News 25: 25-27.
Order Chiroptera. Jn D. E. Wilson and
D. M. Reeder (eds.), Mammal species
of the world, a taxonomic and geograph-
ic reference, 2nd ed., pp. 137-241.
Washington, DC: Smithsonian Institu-
tion Press.
1994. Order of bats; Chiroptera Blumenbach,
1779. Handbook of zoology 8(60): 1-
217.
Koopman, K. F., and G. T. MacIntyre
1980. Phylogenetic analysis of chiropteran
dentition. Jn D. E. Wilson and A. L.
Gardner (eds.), Proceedings of the Fifth
International Bat Research Conference,
pp. 279-288. Lubbock, TX: Texas Tech
Press.
Lapoint, F.-J., and G. Baron

1911.

1993.

1993. Encephalization, adaptation and evo-
lution of bats: statistical evidence for the
monophyly of Chiroptera. Bat Res.
News 33: 64. [Dated 1992 but issued in
1993]

Leche, W.
1875. Zur Kenntniss des Milchgebisses und der

NO. 3103

Zahnhomologien bei Chiroptera. Lunds
Univ. Arsskrift. 14: 1-37.

Zur Anatomie der Beckenregion bei In-
sectivora, mit besonderer Beriicksichti-
gung ihrer morphologischen Beziehun-
ger zu derjenigen anderer Sdugethiere.
Kongl. Svenska Vetenskaps-Akade-
miens Handlingar 20: 1-113.

Le Gros Clark, W. E.

1924. The myology of the tree-shrew (Tupaia
minor). Proc. Zool. Soc. London 1924:
461-497.

On the anatomy of the pen-tailed tree-
shrew (Ptilocercus lowii). Proc. Zool. Soc.
London 1926: 1179-1309.

Luckett, W. P.

1975. Ontogeny of the fetal membranes and
placenta: their bearing on primate phy-
logeny. In W. P. Luckett and F. S. Szalay
(eds.), Phylogeny of the primates, pp.
157-182. New York: Plenum Press.
Ontogeny of amniote fetal membranes
and their application to phylogeny. J”
M. K. Hecht, P. C. Goody, and B. M.
Hecht (eds.), Major patterns in verte-
brate evolution, pp. 439-516. New
York: Plenum Press.
1980a. The suggested evolutionary relation-

ships and classification of tree shrews.
In W. P. Luckett (ed.), Comparative bi-
ology and evolutionary relationships of
tree shrews, pp. 3-31. New York: Ple-
num Press.
1980b. The use of fetal membrane data in as-
sessing chiropteran phylogeny. Jn D. E.
Wilson and A. L. Gardner (eds.), Pro-
ceedings of the Fifth International Bat
Research Conference, pp. 245-265.
Lubbock, TX: Texas Tech Press.
Supraordinal and intraordinal affinities
of rodents. In W. P. Luckett and J.-L.
Hartenberger (eds.), Evolutionary rela-
tionships among rodents, pp. 227-276.
New York: Plenum Press.
Developmental evidence from the fetal
membranes for assessing archontan re-
lationships. Jn R. D. E. MacPhee (ed.),
Primates and their relatives in phylo-
genetic perspective, pp. 149-186. Ad-
vances in primatology series. New York:
Plenum Press.
Luckett, W. P., and J.-L. Hartenberger
1993. Monophyly or polyphyly of the order
Rodentia: possible conflict between
morphological and molecular interpre-
tations. J. Mammal. Evol. 1: 127-147.
MacAlister, A.
1872. The myology of the cheiroptera. Philos.
Trans. R. Soc. London 162: 125-171.

1886.

1926.

1977.

1985.

1993,

1994 SIMMONS: CHIROPTERAN MONOPHYLY 51

MacPhee, R. D. E.

1981. Auditory regions of primates and eu-
therian insectivores: morphology, on-
togeny, and character analysis. Contrib.
Primatol. 18: 1-282.

MacPhee, R. D. E., and M. J. Novacek

1993. Definition and relationships of Lipo-
typhla. Jn F. S. Szalay, M. J. Novacek,
and M. C. McKenna (eds.), Mammal
phylogeny: placentals, pp. 13-31. Ber-
lin: Springer-Verlag.

MacPhee, R. D. E., M. J. Novacek, and G. Storch

1988. Basicranial morphology of Early Terti-
ary erinaceomorphs and the origin of
Primates. Am. Mus. Novitates 2921: 42
pp.

Martin, R. D.

1975. The bearing of reproductive behavior
and ontogeny on strepsirhine phyloge-
ny. In W. P. Luckett and F. S. Szalay
(eds.), Phylogeny of the primates, pp.
265-297. New York: Plenum Press.
Primate origins and evolution. London:
Chapman and Hall.

Matthew, W. D.

1909. The Carnivora and Insectivora of the
Bridger Basin, Middle Eocene. Mem.
Am. Mus. Nat. Hist. 9: 289-567.

Meschinelli, L.

1903. Unnuovo chiroptero fossile (Archaeop-
teropus transiens Meschen.) delle liquiti
di Monteviale. Atti Ist. Veneto Sci. Lett.
Arti. Venezia Cl. Sci. Fis. Mat. Nat. 62:
1329-1344.

Miller, G. S.

1907. The families and genera of bats. Bull.
U.S. Nat. Mus. 57: 1-282.

Mindell, D. P., C. W. Dick, and R. J. Baker

1991. Phylogenetic relationships among
megabats, microbats, and primates.
Proc. Natl. Acad. Sci. USA 88: 10322-
10326.

Miyamoto, M. M., and S. M. Boyle

1989. The potential importance of mitochon-
drial DNA sequence data to eutherian
mammal phylogeny. /n B. Fernholm,
K. Bremer, and H. Jornvall (eds.), The
hierarchy of life, Nobel Symposium 70,
pp. 437-452. Amsterdam: Excerpta
Medica, Elsevier.

Miyamoto, M. M., and M. Goodman

1986. Biomolecular systematics of eutherian
mammals: phylogenetic patterns and
classification. Syst. Zool. 35: 230-240.

Mori, M.

1960. Muskulatur des Pteropus edulis. Okaji-

mas Folia Anat. Japonica 36: 253-307.
Moritz, C., and D. M. Hillis
1990. Molecular systematics: context and

1990.

controversies. In D. M. Hillis and C.

Moritz (eds.), Molecular systematics, pp.

1-10. Sunderland, MA: Sinauer.
Mossman, H. W.

1937. Comparative morphogenesis of the fetal
membranes and accessory uterine struc-
tures. Contrib. Embryol. Carnegie Inst.
Washington 26: 129-246.

1987. Vertebrate fetal membranes. New

Brunswick, NJ: Rutgers Univ. Press.
Novacek, M. J.

1980a. Cranioskeletal features in tupaiids and
selected Eutheria as phylogenetic evi-
dence. Jn W. P. Luckett (ed.), Compar-
ative biology and evolutionary relation-
ships of tree shrews, pp. 35-93. New
York: Plenum Press.

1980b. Phylogenetic analysis of the chiropteran
auditory region. Jn D. E. Wilson and A.
L. Gardner (eds.), Proceedings of the
Fifth International Bat Research Con-
ference, pp. 317-330. Lubbock, TX:
Texas Tech Press.

1985a. Evidence for echolocation in the oldest
known bats. Nature 315: 140-141.

1985b. Cranial evidence for rodent affinities. Jn
W. P. Luckett and J.-L. Hartenberger
(eds.), Evolutionary relationships among
rodents, pp. 59-82. New York: Plenum
Press.

1986. The skull of leptictid insectivorans and
the higher-level classification of euthe-
rian mammals. Bull. Am. Mus. Nat.
Hist. 183: 1-111.

Auditory features and affinities of the
Eocene bats Icaronycteris and Palaeo-
chiropteryx (Microchiroptera, incertae
sedis). Am. Mus. Novitates 2877: 18 pp.
1990. Morphology, paleontology, and the
higher clades of mammals. Jn H. Gen-
oways (ed.), Current mammalogy 2:
507-543. New York: Plenum Press.
1992a. Fossils, topologies, missing data, and the
higher level phylogeny of eutherian
mammals. Syst. Biol. 41: 58-73.
1992b. Fossils as critical data for phylogeny. Jn
M. J. Novacek and Q. D. Wheeler (eds.),
Extinction and phylogeny, pp. 46-88.
New York: Columbia Univ. Press.
1994. Morphological and molecular inroads
to phylogeny. Jn L. Grande and O.
Rieppel (eds.), Interpreting the hierar-
chy of nature: from systematic patterns
to evolutionary process theories, pp. 85-
131. New York: Academic Press.
Novacek, M. J., and A. R. Wyss
1986. Higher level relationships of the Recent
eutherian orders: morphological evi-
dence. Cladistics 2: 257-287.

1987.

52 AMERICAN MUSEUM NOVITATES

Novacek, M. J., A. R. Wyss, and M. C. McKenna
1988. The major groups of eutherian mam-
mals. In M. J. Benton (ed.), The phy-
logeny and classification of the tetra-
pods, pp. 31-71. London: Oxford Univ.

Press (Clarendon).

Nunez, P. E., and C. W. Kilpatrick
In press. Monophyletic or diphyletic origin of

bats as inferred by DNA-DNA hybrid-
ization. Bat Res. News.

Peder, C., and T. Tilley
1969. The retina of a fruit bat. Vision Res. 9:

909-922.

Pettigrew, J. D.

1986. Flying primates? Megabats have the ad-
vanced pathway from eye to midbrain.
Science 231: 1304-1306.

199la. Wings or brain? Convergent evolution
in the origins of bats. Syst. Zool. 40:
199-216.

1991b. A fruitful, wrong hypothesis? Response
to Baker, Novacek, and Simmons. Syst.
Zool. 40: 231-239.

Pettigrew, J. D., and H. M. Cooper
1986. Aerial primates: advanced visual path-

ways in megabats and gliding lemurs.
Soc. Neurosci. Abstr. 12: 1035.

Pettigrew, J. D., and B. G. M. Jamieson

1987. Are flying foxes (Chiroptera: Pteropod-
idae) really primates? Aust. Mammal.
10: 119-124.

Pettigrew, J. D., B. G. M. Jamieson, S. K. Robson,
L. S. Hall, K. I. McAnally, and H. M. Cooper
1989. Phylogenetic relations between micro-

bats, megabats and primates (Mam-
malia: Chiroptera and Primates). Phil-
os. Trans. R. Soc. London B 325: 489-
559.

Pierson, E. D.

1986. Molecular systematics of the Microchi-
roptera: higher taxon relationships and
biogeography. Ph.D. diss., Univ. Cali-
fornia, Berkeley.

Prothero, D. R., E. M. Manning, and M. Fischer
1988. The phylogeny of ungulates. In M. J.

Benton (ed.), The phylogeny and clas-
sification of the tetrapods, vol. 2: mam-
mals, pp. 201-234. Systematics Asso-
ciation Special Volume No. 35B.
Oxford: Clarendon Press.

Rasweiler, J. J.

1979. Early embryonic development and im-
plantation in bats. J. Reprod. Fertil. 56:
403-416.

1990. Implantation, development of the fetal

membranes, and placentation in the
captive black mastiff bat, Molossus ater.
Am. J. Anat. 187: 109-136.

NO. 3103

1992. Reproductive biology of the female black
mastiff bat, Molossus ater. In W. C.
Hamlett (ed.), Reproductive biology of
South American vertebrates, pp. 262-
282. New York: Springer-Verlag.
Reed, C. A.

1951. Locomotion and appendicular anatomy
in three soricoid insectivores. Am. Mid.
Nat. 45: 513-671.

Reinbach, W.

1952. Zur Entwicklung des Primordialcrani-
ums von Dasypus novemcinctus Linné
(Tatusia novemcinctus Lesson) II. Z.
Morphol. Anthropol. 45: 1-72.

Revilliod, P.

1922. Contribution a létude des chiroptéres des
terrains Tertiares 2. Mem. Soc. Paleon-
tol. Suisse 45: 133-195.

Rouse, G. W., and S. K. Robson

1986. Anultrastructural study of megachirop-
teran (Mammalia: Chiroptera) sper-
matozoa: implications for chiropteran
phylogeny. J. Submicrosc. Cytol. 18:
137-152.

Roux, G. H.

1947. The cranial development of certain
Ethiopian “‘insectivores’”’ and its bear-
ing on the mutual affinities of the group.
Acta Zool., Stockholm 28: 165-397.

Russell, D. E., and B. Sigé

1970. Revision des chiroptéres lutétien de
Messel (Hesse, Allemagne). Palaeover-
tebrata 3: 83-182.

Sabeur, G., G. Macaya, F. Kadi, and G. Bernardi

1993. The isochore patterns of mammalian
genomes and their phylogenetic impli-
cations. J. Mol. Evol. 37: 93-108.

Sarich, V. M.

1993. Mammalian systematics: twenty-five
years among their albumins and trans-
ferrins. In F. S. Szalay, M. J. Novacek,
and M. C. McKenna (eds.), Mammal
phylogeny: placentals, pp. 103-114.
Berlin: Springer-Verlag.

Scherer, S.

1990. The protein molecular clock: time for a
reevaluation. In M. K. Hecht, B. Wal-
lace, and R. J. Macintyre (eds.), Evo-
lutionary biology 24: 83-106. New York:
Plenum Press.

Sigé, B.

1991. Morphologie dentaire lactéale d’un chi-

roptére de I’ Eocéne Inférieur-moyen
d’Europe. Geobios 13: 231-236.
Simmons, N. B.

1993. The importanc of methods: archontan
phylogeny and cladistic analysis of mor-
phological data. Jn R. D. E. MacPhee

1994

(ed.), Primates and their relatives in
phylogenetic perspective, pp. 1-61. Ad-
vances in primatology series. New York:
Plenum Press.
Simmons, N. B., M. J. Novacek, and R. J. Baker
1991. Approaches, methods, and the future of
the chiropteran monophyly controver-
sy: areply to J. D. Pettigrew. Syst. Zool.
40: 239-244.
Simpson, G. G.
1945. The principles of classification and a
classification of mammals. Bull. Am.
Mus. Nat. Hist. 85: 1~350.
Slaughter, B. H.
1970. Evolutionary trends of chiropteran den-
titions. Jn B. H. Slaughter and D. W.
Walton (eds.), About bats, pp. 51-83.
Dallas, TX: Southern Methodist Univ.

Press.
Smith, J. D.
1972. Systematics of the chiropteran family
Mormoopidae. Misc. Publ. Univ. Kan-
sas Mus. Nat. Hist. 56: 1-132.
1976. Chiropteran evolution. Jn R. J. Baker,

J. K. Jones, and D. C. Carter (eds.), Bi-
ology of bats of the new world family
Phyllostomatidae, Part I, pp. 49-69.
Lubbock, TX: Spec. Publ. Texas Tech
Univ.
Chiropteran phylogenetics: introduc-
tion. Jn D. E. Wilson and A. L. Gardner
(eds.), Proceedings of the Fifth Inter-
national Bat Research Conference, pp.
233-244. Lubbock, TX: Texas Tech
Press.
Smith, J. D., and G. Madkour
1980. Penial morphology and the question of
chiropteran phylogeny. Jn D. E. Wilson
and A. L. Gardner (eds.), Proceedings
of the Fifth International Bat Research
Conference, pp. 347-265. Lubbock, TX:
Texas Tech Press.
Springer, M. S., and J. A. W. Kirsch
1993. A molecular perspective on the phylog-
eny of placental mammals based on mi-
tochondrial 12S rDNA sequences, with
special reference to the problem of the
Paenungulata. J. Mammal. Evol. 1: 149-
166.
Stanhope, M. J., J. Czelusniak, J.-S. Si, J. Nick-
erson, and M. Goodman
1992. A molecular perspective on mammali-
an evolution from the gene encoding in-
terphotoreceptor retinoid binding pro-
tein. Mol. Phylog. Evol. 1: 148-160.
Stanhope, M. J., W. J. Bailey, J. Czelusniak, M.
Goodman, J.-S. Si, J. Nickerson, J. G. Sgouros,
G. A. M. Singer, and T. K. Kleinschimidt

1980.

SIMMONS: CHIROPTERAN MONOPHYLY 53

1993. A molecular view of primate supraor-
dinal relationships from the analysis of
both nucleotide and amino acid se-
quences. Jn R. D. E. MacPhee (ed.), Pri-
mates and their relatives in phyloge-
netic perspective, pp. 251-292.
Advances in primatology series. New
York: Plenum Press.

Stephens, R. J., and N. Easterbrook

1968. Development of the cytoplasmic mem-
branous organelle in the endodermal
cells of the yolk sac of the bat Tadarida
brasiliensis. J. Ultrastruct. Res. 24: 239-
248.

Stirckler, T. L.

1978. Functional osteology and myology of the
shoulder in the Chiroptera. Contrib.
Vertebr. Evol. 4: 1-198.

Switzer, R. C., J. I. Johnson, and J. A. W. Kirsch

1980. Phylogeny through brain traits: the
course of the dorsal lateral olfactory tract
past the accessory olfactory formation
as a palimpsest of mammalian descent.
Brain Behav. Evol. 17: 339-363.

Swofford, D. L.

1991. When are phylogeny estimates from
molecular and morphological data in-
congruent? In M. M. Miyamoto and J.
Cracraft (eds.), Phylogenetic analysis of
DNA sequences, pp. 295-333. New
York: Oxford Univ. Press.

Szalay, F. S..

1977. Phylogenetic relationships and a clas-
sification of eutherian Mammalia. Jn M.
K. Hecht, P. C. Goody, and B. M. Hecht
(eds.), Major patterns in vertebrate evo-
lution, pp. 315-374. New York: Plenum
Press.

A new appraisal of marsupial phylogeny
and classification. Jn M. Archer (ed.),
Carnivorous marsupials 2: 621-640.
Sydney: R. Soc. of New South Wales.
Arboreality: is it homologous in meta-
therian and eutherian mammals? Jn M.
K. Hecht, B. Wallace, and G. T. Prance
(eds.), Evolutionary biology 18: 215-
258. New York: Plenum Press.

Pedal evolution of mammals in the Me-
sozoic: tests for taxic relationships. Jn
F. 8. Szalay, M. J. Novacek, and M. C.
McKenna (eds.), Mammal phylogeny:
Mesozoic differentiation, multituber-
culates, monotremes, early therians, and
marsupials, pp. 109-128. Berlin:
Springer-Verlag.

Szalay, F. S., and R. L. Decker

1974. Origins, evolution, and function of the
tarsus in late Cretaceous eutherians and

1982.

1984.

1993,

54 AMERICAN MUSEUM NOVITATES NO. 3103

Paleocene Primates. Jn F. A. Jenkins
(ed.), Primate locomotion, pp. 223-259.
New York: Academic Press.
Szalay, F. S., and G. Drawhorn
1980. Evolution and diversification of the Ar-
chonta in an arboreal milieu. Jn W. P.
Luckett (ed.), Comparative biology and
evolutionary relationships of tree
shrews, pp. 133-169. New York: Ple-
num Press.
Szalay, F. S., and S. G. Lucas
1993. Cranioskeletal morphology of archon-
tans, and diagnoses of Chiroptera, Vol-
itantia, and Archonta. In R. D. E.
MacPhee (ed.), Primates and their rel-
atives in phylogenetic perspective, pp.
187-226. Advances in primatology se-
ries. New York: Plenum Press.
Thewissen, J. G. M., and S. K. Babcock
1991. Distinctive cranial and cervical inner-
vation of ming muscles; new evidence
for bat monophyly. Science 251: 934—
936.
1993. The implications of the propatagial
muscles of flying and gliding mammals
for archontan systematics. In R. D. E.
MacPhee (ed.), Primates and their rel-
atives in phylogenetic perspective, pp.
91-109. Advances in primatology se-
ries. New York: Plenum Press.
Thiele, A., M. Vogelsang, and K.-P. Hoffman
1991. Patterns of retinotectal projection in the
megachiropteran bat Rousettus aegyp-
tiacus. J. Comp. Neurol. 314: 671-683.
Van Valen, L.
1979. The evolution of bats. Evol. Theory 4:
104—121.
Vaughan, T. A.
1959. Functional morphology of three bats:
Eumops, Myotis, Macrotus. Univ. Kan-
sas Publ. Mus. Nat. Hist. 12: 1-153.
1970a. The skeletal system. Jn W. A. Wimsatt
(ed.), Biology of bats 1: 97-138. New
York: Academic Press.
1970b. The muscular system. Jn W. A. Wimsatt
(ed.), Biology of bats 1: 139-194. New
York: Academic Press.
Walton, D. W., and G. M. Walton
1970. Post-cranial osteology of bats. Jn B. H.
Slaughter and D. W. Walton (eds.),
About bats: a chiropteran biology sym-
posium, pp. 93-126. Dallas, TX:
Southern Methodist Univ. Press.
Wheeler, W.
In press. Sequence alignment, parameter sen-
sitivity, and the phylogenetic analysis of
molecular data. Syst. Biol.

Wible, J. R.

1984.

1987.

1992.

1993.

Wible, J.
1987.

Wible, J.
1993.

Wible, J.
1988.

The ontogeny and phylogeny of the
mammalian cranial arterial system.
Ph.D. diss., Duke Univ., Durham, NC,
705 pp.

The eutherian stapedial artery: charac-
ter analysis and implications for super-
ordinal relationships. Zool. J. Linn. Soc.
91: 107-135.

Further examination of the basicranial
anatomy of the Megachiroptera: a reply
to A. J. King. Acta Anat. 143: 309-316.
Cranial circulation and relationships of
the colugo Cynocephalus (Dermoptera,
Mammalia). Am. Mus. Novitates 3072:
27 pp.

R., and H. H. Covert

Primates: cladistic diagnosis and rela-
tionships. J. Hum. Evol. 16: 1-22.

R., and J. R. Martin

Ontogeny of the tympanic floor and roof
in archontans. In R. D. E. MacPhee,
Primates and their relatives in phylo-
genetic perspective, pp. 111-148. Ad-
vances in primatology series. New York:
Plenum Press.

R., and M. J. Novacek

Cranial evidence for the monophyletic
origin of bats. Am. Mus. Novitates 2911:
1-19.

Wilson, D. E.

1993.

Order Scandentia. Jn D. E. Wilson and
D. M. Reeder (eds.), Mammal species
of the world, a taxonomic and geograph-
ic reference, 2nd ed., pp. 131-134.
Washington, DC: Smithsonian Institu-
tion Press.

Wise, L. Z., J. D. Pettigrew, and M. B. Calford

1986.

Wyss, A.
1993.

Zeller, U.
1986.

Somatosensory cortical representation
in the Australian ghost bat, Macroder-
ma gigas. J. Comp. Neurol. 248: 257-
262.

R., and J. J. Flynn

A phylogenetic analysis and definition
of Carnivora. In F. S. Szalay, M. J. No-
vacek, and M. C. McKenna (eds.),
Mammal phylogeny: placentals, pp. 32-
52. Berlin: Springer-Verlag.

A.

Ontogeny and cranial morphology of the
tympanic region of the Tupaiidae, with
special reference to Ptilocercus. Folia
Primatol. 47: 61-80.

Zook, J. M., and B. C. Fowler

1982.

Central representation of a specialized
mechanosensory array in the wing of a
bat. Soc. Neurosci. Abstr. 8: 38.

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